(Cestoda: Proteocephalidea) of Synodontis Spp. (Siluriformes)In Africa: Survey of Species and Their Redescriptions

See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/274377313

Tapeworms (Cestoda: Proteocephalidea) of Synodontis spp. (Siluriformes)in Africa: Survey of species and their redescriptions

ARTICLE in ZOOTAXA · JULY 2011 Impact Factor: 0.91

CITATIONS READS 6 17

5 AUTHORS, INCLUDING:

Alain De Chambrier Tomas Scholz Natural History Museum of Geneva Institute of Parasitology Biology Centre, ASCR

104 PUBLICATIONS 809 CITATIONS 288 PUBLICATIONS 3,443 CITATIONS

SEE PROFILE SEE PROFILE

Zuheir Mahmoud University of Khartoum

47 PUBLICATIONS 69 CITATIONS

SEE PROFILE

Available from: Alain De Chambrier Retrieved on: 10 January 2016 TERMS OF USE This pdf is provided by Magnolia Press for private/research use. Commercial sale or deposition in a public library or website is prohibited.

Tapeworms (Cestoda: Proteocephalidea) of Synodontis spp. (Siluriformes) in Africa: survey of species and their redescriptions

ALAIN DE CHAMBRIER1, TOMÁŠ SCHOLZ2, ZUHEIR N. MAHMOUD3, JEAN MARIAUX1 & MILOSLAV JIRKŮ2 1Department of Invertebrates, Natural History Museum, P.O. Box 6434, CH-1211 Geneva 6, Switzerland. E-mail: [email protected] 2Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, Branišovská 31, 370 05 České Budějovice, Czech Republic. E-mail: [email protected] 3Department of Zoology, Faculty of Science, University of Khartoum, Khartoum, Sudan. E-mail: [email protected]

Abstract

Proteocephalidean tapeworms parasitic in Synodontis spp. (Siluriformes: Mochokidae) in Africa are critically reviewed based on examination of their type specimens and extensive new material from Kenya and Sudan. Proteocephalus synodontis Woodland, 1925 and Proteocephalus membranacei Troncy, 1978 are considered to be valid and both species are redescribed. Proteocephalus synodontis differs from congeners parasitic in other African freshwater fishes, including P. membranacei, in the possession of an extraordinarily developed inner longitudinal musculature formed by massive bundles of muscle fibres. A considerable variability was found in the size (35–140 × 30–75 μm) and shape (from elongate, tear-shaped to spherical) of the apical organ, which was present in all specimens from the Nile River basin in the Sudan, but absent in all but two juvenile specimens from Lake Turkana in Kenya. A congruent low molecular variability was also observed and these slight morphological and genetic differences may indicate ongoing allopatric speciation of tapeworms from the two previously connected basins. Nevertheless, all tapeworms were identical in all other morphological and molecular characteristics and are considered conspecific. Proteocephalus largoproglottis Troncy, 1978 from Synodontis membranacea from Lake Chad is synonymized with P. membranacei described from the same host and locality. Proteo- cephalus synodontis and P. membranacei differ from each other in the development of the inner longitudinal musculature, shape of the scolex and presence of weakly developed, almost indistinguishable ventral osmoregulatory canals in the latter species.

Key words: Proteocephalus, Proteocephalidae, Synodontis spp., freshwater fish, Africa, Nile, Turkana, taxonomy, allopatric speciation, 28S rDNA, 5.8S/ITS2

Introduction

African freshwater fishes have been reported to harbour 19 species of the order Proteocephalidea, ten of which belong to the genus Proteocephalus Weinland, 1858 (Khalil & Polling 1997; de Chambrier et al. 2009). To date, three species of Proteocephalus have been described from catfish of the genus Synodontis Cuvier, 1816 (Siluri- formes: Mochokidae) from Africa, namely Proteocephalus synodontis Woodland, 1925 from Synodontis schall (Bloch and Schneider) from the Nile River in Khartoum, Sudan, and Proteocephalus largoproglottis Troncy, 1978 and Proteocephalus membranacei Troncy, 1978, both from Synodontis membranacea (Geoffroy Saint Hillaire) from Lake Chad in Ndjamena, Chad (Woodland 1925; Troncy 1978). A fourth species, Proteocephalus beau- champi Fuhrmann and Baer, 1925, has been reported by Khalil (1963) from S. schall from the Sudan. This species is known to be a parasite of Chrysichthys spp. (Siluriformes: Bagridae) and no voucher exists for this material. This determination is thus dubious and cannot be confirmed. Morphological descriptions of all these species were incomplete and lacked much information on taxonomi- cally and phylogenetically important features. Recently, tapeworms apparently conspecific with P. synodontis were collected from the type host, S. schall, and other Synodontis spp. from several localities of the Nile River basin in

Accepted by N. Dronen: 14 Jun. 2011; published: 26 Jul. 2011 1 TERMS OF USE This pdf is provided by Magnolia Press for private/research use. Commercial sale or deposition in a public library or website is prohibited. the Sudan, including the type locality for P. synodontis (Khartoum), and from Lake Turkana in Kenya. This material, together with data based on examination of the type specimens of all three Proteocephalus species described from Synodontis spp., i.e. P. synodontis, P. largoproglottis and P. membranacei, enabled us to critically review tax- onomic status of these tapeworms and to provide redescriptions of the species considered to be valid.

Material and methods

Data on the material studied, its origin (hosts and localities) and specimens deposited are provided in TABLE 1 and Appendix 1. Newly collected tapeworms were obtained from the intestine of live or fresh fish hosts and rinsed in saline. Specimens were fixed with hot 4% (almost boiling) neutral formaldehyde solution (formalin), immediately removed and stored in new 4% formalin for a few weeks, then stored in 70% ethanol. A fragment of the strobila of most specimens was preserved in 99% molecular grade ethanol for DNA sequencing. The specimens for morphological study were processed as described in previous papers (de Chambrier 2001; de Chambrier et al. 2008, 2009; Oros et al. 2010). Microthrix terminology follows that of Chervy (2009). All measurements in descriptions are given in micrometres (µm) unless otherwise stated. Partial sequences from the 28SrDNA and 5.8S/ITS2 genes were obtained and analyzed following published protocols (Zehnder & Mariaux 1999; Hypša et al. 2005). Fish hosts from the Sudan were identified by local ichthyologists, including one of the authors (ZNM), whereas those from Kenya by Dr. Radim Blažek from the Institute of Vertebrate Biology, AS CR, Brno, Czech Republic. List and coordinates of sampling localities: Khartoum, Sudan (type-locality), 15°35'03"N, 32°32'13"E; Kostí (White Nile), Sudan, 13°10'20"N, 32°40'20"E; Sennar Dam (Blue Nile), Sudan, 13°32'37"N, 33°38'12"E; Khashm el-Girba (dam on the Atbarah River), Sudan, 14°55'10"N, 35°54'07"E; El-Molo Bay (Loiyangalani area), Lake Turkana, Kenya, 2°50'00"N, 36°41'50"E; Kalokol (Longech village), Lake Turkana, Kenya, 3°33'17"N, 35°54'56"E; Omo River Delta (Todonyang), Lake Turkana, Kenya, 4°27'10"N, 35°56'30"E. Abbreviations used in descriptions are as follows: x = mean; n = number of measurements; CV = coefficient of variability (CV = x/SD × 100 in %; SD = standard deviation); OV = ratio of the width of the ovary to the width of the proglottis (in %); RLCS = ratio of the length of the cirrus-sac to the width of the proglottis (in %). Acronyms of collections: BMNH = The Natural History Museum, London, UK; HWML = H. W. Manter Laboratory, University of Nebraska State Museum, Lincoln, USA; IPCAS = Institute of Parasitology, České Budějovice, Czech Republic; MHNG = Natural History Museum of Geneva, Switzerland; MNHNP = National Museum of Natural History of Paris, France; USNPC = U.S. National Parasite Collection, Beltsville, USA.

Results

Survey of species and their redescriptions

On the basis of a critical examination of the type material of three Proteocephalus spp. from Synodontis spp., P. synodontis and P. membranacei are considered valid and their redescriptions are provided, whereas P. largoproglottis is synonymized with P. membranacei.

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).

2 · Zootaxa 2976 © 2011 Magnolia Press de CHAMBRIER ET AL. TERMS OF USE This pdf is provided by Magnolia Press for private/research use. Commercial sale or deposition in a public library or website is prohibited. A. (26%) (23%) (%) (19%) (21%) (14%) (1%) (75%) (25%) 6/32 6/32 36/138 36/138 3/4 3/4 1/4 23/102 4/19 4/19 3/22 3/22 1/68 1/68 Totals 76/321 (24%) (24%) 76/321 (n = 1) from Blue Blue = 1) from (n and those from from those and S. sorex S. sorex (%) (%) Turkana Turkana Sub-totals (21%) (21%) A. acuticeps to (n = 1) and = 1) and (n S. filamentosa (n = 3) from White Nile at el-Renk. ** Nile at el-Renk. White = 3) from (n as identified Originally El-Molo Kalokol Todonyang 15/34 4/30 4/30 15/34 4/44 23/108 S. schall S. schall (%) (%) (25%) (25%) Nile Sub-totals (n = 1) and = 1) and (n S. nigrita S. nigrita therefore herein, specimens from Nile are tentatively assigned Nile are tentatively from specimens herein, therefore Khashm Khashm el-Girba from Khartoum (n = 1) and White Nile at Kostí (n = 4), Nile at Kostí (n White = 1) and (n Khartoum from examined from individual localities (No. infected/No. examined). Sample sizes indicate pooled data from 2006, 2008 & 2006, 2008 & pooled data from indicate sizes Sample examined). (No. infected/No. localities individual from examined S. batensoda S. batensoda (n = 4) from White Nile at Kostí, and Nile at Kostí, and White = 4) from (n were negative: - 3/4 - - 3/4 (75%) ------(75%) - (25%) (21%) Khartoum Kostí Sennar - 3/4 4/35 - 3/4 12/58 1/11 1/4 7/12 - 1/4 (25%) - 3/5 1/12 11/44 7/27 - 0/12 1/2 3/5 4/19 (21%) - - - - (21%) - - 4/19 3/5 1/2 0/12 2/17 1/5 - 3/22 (14%) ------(14%) - - 1/5 2/17 3/22 0/3 0/18 1/17 0/4 1/42 (2%) 0/2 0/5 0/19 0/19 (2%) 0/5 0/2 0/26 0/3 0/4 1/17 0/18 1/42 Proteocephalus synodontis synodontis Proteocephalus Synodontis ) 1/7 1/16 4/9 - 6/32 (19%) - - - - (19%) - - 4/9 1/16 1/7 6/32 ) cf. cf. S. membranacea S. membranacea . only 3/15 15/94 19/51 16/53 53/213 acuticeps schall (type host) (type 2/8 8/33 10/30 5/17 (28%) 25/88 8/22 3/19 0/9 (22%) 11/50 cf. cf. , but this species occurs in Western Africa only (Retzer 2010) – (Retzer only Africa Western in occurs species this , but sp. (cf. Numbers of hosts of A. sacchii Synodontis Auchenoglanis Auchenoglanis (Turkana)** occidentalis Turkana to Turkana Nile at Wad Medani, Nile at Wad Medani, (Nile) & (Nile) & Auchenoglanis Auchenoglanis sacchii 2010 for the Sudan (Nile basin) and from 2008 & 2009 for Kenya (Turkana), respectively. respectively. (Turkana), Kenya 2009 for 2008 & from and basin) (Nile Sudan the 2010 for Country – basin schall Synodontis Sudan – Nile* euptera Synodontis frontosa Synodontis Kenya – Turkana TABLE 1. Host caudovittata Synodontis *The following species of Synodontis nigrita nigrita Synodontis Synodontis serrata serrata Synodontis Synodontis Synodontis Totals –

PROTEOCEPHALIDS FROM AFRICAN SILURIFORMES Zootaxa 2976 © 2011 Magnolia Press · 3 TERMS OF USE This pdf is provided by Magnolia Press for private/research use. Commercial sale or deposition in a public library or website is prohibited.

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, Sudan— localities 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. Prolifer- ative 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 chro-

4 · Zootaxa 2976 © 2011 Magnolia Press de CHAMBRIER ET AL. TERMS OF USE This pdf is provided by Magnolia Press for private/research use. Commercial sale or deposition in a public library or website is prohibited. mophilic 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 nucle- otide. 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 endor- heic 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).

PROTEOCEPHALIDS FROM AFRICAN SILURIFORMES Zootaxa 2976 © 2011 Magnolia Press · 5 TERMS OF USE This pdf is provided by Magnolia Press for private/research use. Commercial sale or deposition in a public library or website is prohibited.

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 1116H; 9, 10); P. largoproglottis (= syn. of P. m em- branacei), syntype (MNHNP 1115H; 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).

6 · Zootaxa 2976 © 2011 Magnolia Press de CHAMBRIER ET AL. TERMS OF USE This pdf is provided by Magnolia Press for private/research use. Commercial sale or deposition in a public library or website is prohibited.

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 Syno- dontis 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. Abbrevi- ations: 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; uo— uterine 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).

PROTEOCEPHALIDS FROM AFRICAN SILURIFORMES Zootaxa 2976 © 2011 Magnolia Press · 7 TERMS OF USE This pdf is provided by Magnolia Press for private/research use. Commercial sale or deposition in a public library or website is prohibited.

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 1116H); Fig. 35—syntype of P. largoproglottis (= syn. of P. membranacei; MNHNP 1115H). 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; uo— uterine 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).

8 · Zootaxa 2976 © 2011 Magnolia Press de CHAMBRIER ET AL. TERMS OF USE This pdf is provided by Magnolia Press for private/research use. Commercial sale or deposition in a public library or website is prohibited.

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 1116H); Fig. 40—syntype of P. largoproglottis (= syn. of P. membranacei; MNHNP 1115H). Abbreviations: em—embryophore; oe—outer envelope; on—oncosphere. Scale bars = 20 µm.

PROTEOCEPHALIDS FROM AFRICAN SILURIFORMES Zootaxa 2976 © 2011 Magnolia Press · 9 TERMS OF USE This pdf is provided by Magnolia Press for private/research use. Commercial sale or deposition in a public library or website is prohibited.

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 reg- ular occurrence in a bagrid definitive host.

Proteocephalus membranacei Troncy, 1978 (Figures 9–13, 34, 35, 39, 40; see also Troncy 1978—figs. 6 [P. membranacei] & 7 [P. largoproglottis])

Syn.: Proteocephalus largoproglottis Troncy, 1978 (new synonym)

Type-and only host. Synodontis membranacea (Geoffrey Saint Hillaire, 1809) (Siluriformes: Mochokidae). Type locality. Lake Chad in Ndjamena, Chad. Type material. MNHNP (1116H). Geographical distribution. Lake Chad. Redescription. Based on type specimens; measurements of P. largoproglottis in parentheses. Proteocephali- dae, Proteocephalinae. Strobila with acraspedote proglottides, 154–162 (70–86) mm long and up to 2.8 (1.6) mm wide, consisting of 110–121 (138) proglottides: 57–66 (71) immature, only 1–3 (2) mature, 25–27 (22) pregravid and 14–38 (43) gravid. Proglottides variable in shape, from almost rectangular to much longer than wide (much wider than long to slightly longer than wide in gravid proglottides). Longitudinal internal musculature well developed, forming wide band of isolated muscle fibres. Osmoregula- tory canals, including ventral ones, difficult to observe, visible only in some cross sections of mature proglottides (Fig. 34). Scolex unarmed, slightly wider than neck, 500–525 (600) wide, rounded (Figs. 9–11, 13), with four uniloculate suckers, opening sublaterally on dorsal and ventral sides of scolex (Figs. 10–13). Apical organ widely oval, thin- walled, 35–50 (35–40) long and 30–35 (30–35) wide, difficult to observe due to high concentration of glands cells in apex of scolex. Proliferative zone 0.4–1.6 mm long and 270–375 wide. Scolex and proliferative zone uniformly covered with short, dense papilliform filitriches. Testes medullary, spherical to oval, 65–85 long and 50–65 wide, 200–250 (150–200) in number according to original description (precise number could not be counted reliably in type specimens), usually in one layer, with a few testes in second incomplete layer in cross section (Fig. 35). Testes forming two fields confluent anteriorly, present also in gravid proglottides. External vas deferens coiled, occupying narrow field, reaching, but never overlapping, midline of proglottis aporally. Cirrus-sac elongated, thin-walled, 130–160 (210–270) long and 60–100 wide (length/width ratio = 2.5–4.1). RLCS = 12–16% (14–17%). Internal vas deferens thin-walled; ejaculatory duct thick-walled, long, forming several loops; cirrus unarmed, long, may occupy more than half-length of cirrus- sac. Genital pore irregularly alternating, almost equatorial, situated at 42–47% (46–52%) of proglottis length. Gen- ital atrium shallow. Ovary medullary, bilobed. OV = 55–59% (56–60%). Mehlis’ glands about 100–105 in diameter. Vagina anterior 60% (40%) or posterior 40% (60%; n = 40) to cirrus-sac, with concentration of chromophilic cells in its distal part, surrounded by weakly developed muscles fibres near genital pore. Vitelline follicles medullary in two longitudinal bands on both sides of proglottis, occupying almost its total length. Uterus medullary, with type 1 development according to de Chambrier et al. (2004), with lumen of uterus appearing in last immature proglottides, gradually extending to form tubular structure. Eggs appear simultaneously with formation of lateral, thick-walled diverticula lined with chromophilic cells. In gravid proglottides, lateral diverticula remain thin-walled, 15–23 (9–16) in number on each side, occupying up to 71% of proglottis width; they open by two or three uterine longitudinal orifices.

10 · Zootaxa 2976 © 2011 Magnolia Press de CHAMBRIER ET AL. TERMS OF USE This pdf is provided by Magnolia Press for private/research use. Commercial sale or deposition in a public library or website is prohibited. 5 diverticula 4 position 3 ratio of the distance of the genital genital the of distance ratio the of 3 after Troncy (1978). Troncy after pore 1 P. largoproglottis P. largoproglottis relative size relative 1 ) in Africa. Africa. ) in and and Auchenoglanis P. membranacei and and Synodontis anterior/posterior position of the distal part of the vagina to the cirrus–sac (expressed in % as (expressed cirrus–sac in to the vagina anterior/posterior distal part the the position of of 4 ratio of the total width of the ovary to the width of the proglottis %); the of (in width to the ovary the of total width ratio the of

spp. from catfish ( catfish from spp. 2 Proteocephalus number of diverticula on each side. Number of testes of of testes of Number side. each on diverticula of number 5 – Chad, Lake Chad– Chad, Lake – Chad, Lake Chad– Chad, Lake 640–810 245–340 65–70 39–45 435–680 100–111 16–25 58–66 42–58 42–58 10–16 42–58 4–12 16–25 58–66 42–58 53–47 100–111 6–9 13–19 56–66 37–48 435–680 30–70 11–14 95–132 40–60 7–11 39–45 65–70 117 400–660 - 41–56 72–28 390 11–14 66–69 41–50 245–340 56–60 16–21 40–90 625–755 130 75 640–810 60–120 43–50 57–64 770 330–340 285–355 50–100 12–17 7–9 90–160 780–960 84–16 60 118–133 275–345 705 740 535 115 35 285–315 120 65 14–18 60–66 40–46 920–1010 910 385–405 655–1310 250–530 absent absent 455–645 111–137 12–30 52–67 39–60 56–44 5–15 56–44 8–12 35–65 12–30 52–67 39–60 111–137 12–15 61–68 44–56 109–123 455–645 absent 525–545 absent 250–530 absent absent 655–1310 325–355 885–890 Scolex Suckers Apical organ Neck Number Cirrus-sac Ovary Genital Vagina Uterine organ Vagina Ovary Genital Cirrus-sac Number Neck Apical Scolex Suckers width width diameter length width width testes of size relative – Turkana Kenya, Lake – Sudan, Nile River Nile – Sudan, 495–520 225–260 50 35 375 200–250 12–16 55–59 42–47 40–60 15–25 40–60 12–16 55–59 42–47 50 375 200–250 35 225–260 495–520 600 275–280 40 35 - 150–200 14–17 56–60 46–52 60–40 9–16 60–40 40 600 - 14–17 56–60 46–52 35 275–280 150–200 Selected measurements of adult specimens of of specimens adult of Selected measurements (type host) host) (type Fish host host Fish . acuticeps . acuticeps Species – locality – locality Species cf S. euptera S. euptera S. frontosa S. nigrita S. serrata A.. synodontis Proteocephalus Type material 620 280–320 160 120 380 - 19 58–69 44–55 61–39 7–12 61–39 - 380 19 44–55 (1886) 160 120 58–69 material synodontis Proteocephalus 547 620 280–320 298 S. schall - Fritsch - 373 - Type - 1 – Appendix Vouchers 14–33 65–67 42 ~20 S. caudovittata 620–880 200–345 140 80 425–910 103–133 16–21 56–64 38–53 47–53 6–11 S. schall S. schall S. membranacea largoproglottis Proteocephalus S. frontosa S. frontosa Proteocephalus membranacei S. membranacea ratio of the length of the cirrus–sac to the width of the proglottis %); the of (in width to cirrus–sac the the of length ratio the of minimum–maximum for individual specimens); TABLE 2. 1 pore from the anterior margin of the proglottis to the total length of the proglottis %); the of (in proglottis the total of to length the margin anterior the pore from

PROTEOCEPHALIDS FROM AFRICAN SILURIFORMES Zootaxa 2976 © 2011 Magnolia Press · 11 TERMS OF USE This pdf is provided by Magnolia Press for private/research use. Commercial sale or deposition in a public library or website is prohibited.

Eggs with membraneous outer envelope with paired lateral auricular projections (Figs. 39, 40), 47–58 long and 25–27 wide; embryophore thick, spherical to slightly subspherical, long 23–25 long and 21–24 wide, containing granular, usually incomplete internal envelope (Figs. 39, 40); oncospheres oval, 12–15 long and 10–12 wide, with six embryonic hooks about 6 long (Figs. 39, 40). Remarks. Quality of type material of both species described by Troncy (1978), i.e. Proteocephalus largoproglottis and P. membranacei (MNHNP 1115H and 1116H), is poor and it was not possible to use it for making new illustrations (Troncy 1978 provided only a few line drawings of both species—see his figs. 6 & 7). However, it was possible to observe internal morphology and to reveal that both taxa are indistinguishable in all but one morphological characteristics. Among others, they share an identically shaped scolex, with a very small, thin-walled apical organ and a similar structure of the inner longitudinal musculature; their osmoregulatory canals, including ventral ones, are indistinguishable in mature, pregravid and gravid proglottides, and their eggs with lateral processes are also identical. Both species only differ by the shape of their proglottides, those of P. membranacei being elongate, much longer than wide, whereas those of P. largoproglottis being short and wide (see figs. 6A, B and 7A, B, D in Troncy 1978). However, this difference seems to reflect a different state of contraction of the worms when they were fixed. The tapeworms described as P. membranacei were probably already dead when fixed, because they were too relaxed and thus became more elongate; their internal organs are difficult to observe because of decomposition of the tissues. Troncy (1978) admitted poor quality of these specimens (“État de conservation médiocre”). In contrast, worms described as P. largoproglottis are strongly contracted and thus their proglottides are much wider than long. Contraction of the material was also mentioned by Troncy (1978—“Les spécimens sont en général rétractés”). Previous studies on Proteocephalus tapeworms (e.g. those parasitic in European fish–Scholz and Hanzelová, 1998), revealed a considerable intraspecific variability of several taxa in proglottis shape. Similarly, proglottides of congeneric cestodes from African catfish, namely P. glanduligerus from Clarias spp. (Scholz et al. 2009) and P. synodontis (this study) were highly variable in their shape (even in the same worm). Therefore, the shape of proglottides is not considered to represent a character that would justify the validity of the tapeworms described by Troncy (1978) as two separate species. As a result, P. largoproglottis, the description of which appeared later (pp. 542–546), is synonymized with P. membranacei, which was described first (pp. 538–542).

Discussion

The present study has revealed that only two instead of three species of Proteocephalus parasitize Synodontis spp. in Africa. Both species share some morphological features not present in congeneric taxa, such as a well developed inner longitudinal musculature (even though that of P. membranacei is much less developed than that of P. synodontis) and their eggs possess two lateral projections (Figs. 36–40). Similar projections, the form of which is species-specific, were observed in Rudolphiella tapeworms from the Neotropical catfish and in Proteocephalus glanduligerus (Janicki, 1928), a parasite of Clarias catfish in Africa (Gil de Pertierra & de Chambrier 2000; Scholz et al. 2009). Both Proteocephalus species from Synodontis spp. can be distinguished from each other by the following morphological characteristics: (a) the inner longitudinal musculature is much less developed in P. membranacei, in which it is formed by isolated muscle fibres (Figs. 34, 35), than in P. synodontis, in which fibres form a large bundles tightly grouped together (Figs. 27, 28); (b) the scolex of P. membranacei is spherical, without deep lobes around suckers, and lacks wrinkles in its posterior part (Figs. 9–13), whereas the scolex of P. synodontis is pyramidal, in form of a four-sided truncated cone, with suckers deeply embedded within lobes and the posterior part of the scolex longitudinally wrinkled (Figs. 1–6); (c) ventral osmoregulatory canals of P. synodontis are well developed and easy to see in all proglottides, including gravid ones (Figs. 30, 32), whereas those of P. membranacei are difficult to observe or almost indistinguishable even in mature proglottides and cross sections (Fig. 35); (d) lateral fields of testes of P. membranacei are not completely separated as in P. synodontis, but are confluent near the anterior margin of proglottides (even though Troncy, 1978 illustrated in figures 7A and 7B testicular fields as being separated); (e) number of testes is lower (95–133) in P. synodontis compared to P. membranacei (allegedly 150– 250 testes, but poor quality of the type material casts doubts upon reliability of the data provided by Troncy 1978).

12 · Zootaxa 2976 © 2011 Magnolia Press de CHAMBRIER ET AL. TERMS OF USE This pdf is provided by Magnolia Press for private/research use. Commercial sale or deposition in a public library or website is prohibited.

Acknowledgments

The authors are obliged to Dia-Eldin Elnaiem (Davis, University of California), who helped organize the stay of A. de C. and T. S. in the Sudan in 2006, André Piuz for providing SEM photomicrographs, and Janik Pralong, Flor- ence Marteau and Gilles Roth (all Geneva) for their help with drawings and laboratory assistance. The field work in the Sudan and Kenya would not have been possible without the invaluable help of Radim Blažek (Institute of Ver- tebrate Biology, Czech Republic), Musa Mohammed Abdelrahman, Sayed Yousif Osman Elsheikh, Huda Ahmed Hassan and Zuhal Ahamed Abdallah Omer (all Faculty of Science, University of Khartoum), Khalid Bashir Abaker and Ammar Osmar (White Nile Fisheries Research Station in Kostí), Harrison Charo-Karisa, David Lotuliakou and John Malala (all from the Kenya Marine and Fishery Research Institute, Kisumu Centre and KMFRI Kalokol Field Station). The support of the Embassy of Switzerland in Khartoum (Ambassador Andrea Reichlin) is also acknowl- edged. This project was supported in part by the National Science Foundation PBI award Nos. 0818696 and 0818823. A. de C. is also deeply indebted to the “Donation Georges and Antoine Claraz” for supporting this study. T. S. and M. J. acknowledge financial support of the Grant Agency of the Czech Republic (project No. 524/08/ 0885), Institute of Parasitology (projects Nos. Z60220518 and LC 522), and Grant Agency of the Academy of Sci- ences of the Czech Republic (project No. KJB 600960813).

References de Chambrier, A. (1988) Crepidobothrium garzonii n. sp. (Cestoda: Proteocephalidae) parasite de Bothrops alternatus Dum. Bibr. & Dum., 1854 (Serpentes: Viperidae) au Paraguay. Revue Suisse de Zoologie, 95, 1163–1170. de Chambrier, A. (1989a) Révision du genre Crepidobothrium Monticelli, 1900 (Cestoda: Proteocephalidae) parasite d’ophidi- ens néotropicaux. I. C. gerrardii (Baird, 1860) et C. viperis (Beddard, 1913). Revue Suisse de Zoologie, 96, 191–217. de Chambrier, A. (1989b) Révision du genre Crepidobothrium Monticelli, 1900 (Cestoda: Proteocephalidae) parasite d’ophidi- ens néotropicaux. II. C. dollfusi Freze, 1965, C. lachesidis (MacCallum, 1921) et conclusions. Revue Suisse de Zoologie, 96, 345–380. de Chambrier, A. (2001) A new tapeworm from the Amazon, Amazotaenia yvettae gen. n., sp. n. (Eucestoda: Proteocephalidea) from the siluriform fishes Brachyplatystoma filamentosum and B. vaillanti (Pimelodidae). Revue Suisse de Zoologie, 108, 303–316. de Chambrier, A., Mariaux, J., Sène, A., Mahmoud, Z.N. & Scholz, T. (2008) Sandonella sandoni (Lynsdale, 1960), an enig- matic and morphologically unique cestode parasitic in the osteoglossiform fish Heterotis niloticus in Africa. Journal of Parasitology, 94, 202–211. de Chambrier, A., Scholz , T., Beletew, M. & Mariaux, J. (2009) A new genus and species of proteocephalidean (Cestoda) from Clarias catfishes (Siluriformes: Clariidae) in Africa. Journal of Parasitology, 95, 160–168. de Chambrier, A., Scholz, T. & Vaucher, C. (1996) Tapeworms (Cestoda: Proteocephalidea) of Hoplias malabaricus (Pisces: Characiformes, Erythrinidae) in Paraguay: description of Proteocephalus regoi sp. n., and redescription of Nomimoscolex matogrossensis. Folia Parasitologica, 43, 133–140. de Chambrier, A. & Vaucher, C. (1999) Proteocephalidae et Monticelliidae (Eucestoda: Proteocephalidea) parasites de poissons d’eau douce au Paraguay, avec descriptions d’un genre nouveau et de dix espèces nouvelles. Revue Suisse de Zoologie, 106, 165–240. de Chambrier, A., Zehnder, M.P., Vaucher, C. & Mariaux, J. (2004) The evolution of the Proteocephalidea (Platyhelminthes, Eucestoda) based on an enlarged molecular phylogeny, with comments on their uterine development. Systematic Parasi- tology, 57, 159–171. de Chambrier, S. & de Chambrier, A. (2010) Two new genera and two new species of proteocephalidean tapeworms (Euces- toda) from reptiles and amphibians in Australia. Folia Parasitologica 57, 263–279. Chervy, L. (2009) Unified terminology for cestodes microtriches: a proposal from the International Workshops on Cestode Sys- tematics in 2002–2008. Folia Parasitologica, 56, 199–230. Dgebuatze, Y.Y., Golubtsov, A.S., Mikheev, V.N. & Mina, M.V. (1994) Four new species of the Omo-Turkana basin, with comments on the distribution of Nemacheilus abyssinicus (Cypriniformes: Balitoridae) in Ethiopia. Hydrobiology, 286, 125– 128. Froese, R. & Pauly, D. (Eds.) (2011) FishBase. World Wide Web electronic publication. www.fishbase.org, April 2011. Gil de Pertierra A.A. & de Chambrier A. (2000) Rudolphiella szidati sp. n. (Proteocephalidea: Monticellidae, Rudolphiellinae) parasite of Luciopimelodus pati (Valenciennes, 1840) (Pisces: Pimelodidae) from Argentina with new observations on Rudolphiella lobosa (Riggenbach, 1895). Revue Suisse de Zoologie, 107, 81–95. Harvey, C.P.D. & Grove A.T. (1982) A prehistoric source of the Nile. Geographic Journal, 148, 327–336. Hopson, A.J. (ed). (1982) Lake Turkana: a report on the finding of the Lake Turkana project 1972–1975. Vols. 1–6. Overseas Development Administration, London.

PROTEOCEPHALIDS FROM AFRICAN SILURIFORMES Zootaxa 2976 © 2011 Magnolia Press · 13 TERMS OF USE This pdf is provided by Magnolia Press for private/research use. Commercial sale or deposition in a public library or website is prohibited.

Hypša, V., Škeříková, A. & Scholz T. (2005) Phylogeny, evolution and host-parasite relationships of the order Proteocephalidea (Eucestoda) as revealed by combined analysis and secondary structure characters. Parasitology 130: 359–371 Khalil, L.F. (1963) On some proteocephalid cestodes from freshwater fishes in the Sudan. Journal of Helminthology 37, 307– 318. Khalil, L.F. & Polling, L. (1997) Check list of the helminth parasites of African freshwater fishes. University of the North, Piet- ersburg, Republic of South Africa, 185 pp. Kuchta, R., Scholz, T., Brabec, J. & Bray, R. A. (2008a) Suppression of the tapeworm order Pseudophyllidea (Platyhelminthes: Eucestoda) and the proposal of two new orders, Bothriocephalidea and Diphyllobothriidea. International Journal for Par- asitology, 38, 49–55. Kuchta, R., Scholz, T. & Bray, R.A. (2008b) Revision of the order Bothriocephalidea Kuchta, Scholz, Brabec & Bray, 2008 (Eucestoda) with amended generic diagnoses and keys to families and genera. Systematic Parasitology, 71, 81–136. Oros, M., Scholz, T. & Hanzelová, V. (2010) Scolex morphology of monozoic cestodes (Caryophyllidea) from the Palaearctic Region: a useful tool for species identification. Folia Parasitologica 57, 37–46. Retzer, M.E. (2010) Taxonomy of Auchenoglanis Gunther, 1865 (Siluriformes: Auchenoglanididae). Zootaxa, 2655, 25-51. Scholz, T., de Chambrier, A., Beletew, M. & Mahmoud, Z.N. (2009) Redescription of Proteocephalus glanduligerus (Janicki, 1928) Fuhrmann, 1933 (Cestoda: Proteocephalidea), a parasite of Clarias catfishes in Africa with a unique glandular apical organ. Journal of Parasitology, 95, 443–449. Scholz, T. & Hanzelová, V. (1998) Tapeworms of the genus Proteocephalus Weinland, 1858: Proteocephalidae, parasites of fishes in Europe. Studie AV ČR, Academia, Prague, No. 2, 119 pp. Scholz, T., Hanzelová, V., Škeříková, A., Shimazu, T. & Rolbiecki, L. (2007) An annotated list of species of the Proteocephalus Weinland, 1858 aggregate sensu de Chambrier et al. (2004) (Cestoda: Proteocephalidea), parasites of freshwater fishes in the Palaearctic Region, their phylogenetic relationships and key to identification. Systematic Parasitology 67, 139–156. Troncy, P.M. (1978) Nouvelles observations sur les parasites des poissons du bassin Chadien. Bulletin de l’Institut Fondamental d’Afrique Noire, 40, 536–546. Woodland, W.N.F. (1925) On three new proteocephalids (Cestoda) and a revision of the genera of the family. Parasitology, 17, 370–394. Zehnder, M.P. & Mariaux J. (1999) Molecular systematic analysis of the order Proteocephalidea (Eucestoda) based on mitochon- drial and nuclear rDNA sequences. International Journal for Parasitology 29, 1841–1852.

APPENDIX 1. Comparative material examined.

Types: Holotype (designated as cotype) of Proteocephalus synodontis—BMNH 1961.4.10.87–102; syntypes of P. largoproglottis—MNHNP 1115H; syntypes of P. membranacei—MNHNP 1116H.

Voucher material of Proteocephalus synodontis (collection numbers of MHNG INVE in parentheses, unless otherwise stated; for acronyms—see Materials & Methods): Nile Basin, Sudan. Synodontis schall (type-host): Khartoum (type-locality), fish market, 21.iii.2006—two tapeworms from fish of field Nos. Sud 24 (MHNG INVE 50009) & 27 (50010); White Nile in Kostí, 16. & 17.xi.2008 & 3.ii.2010—nine spec. from Sud 230 (62920), 242 (62921), 244 (no voucher), 245 (62922, 62923), 246 (IPCAS C-512), 257 (62926) & 693 (69926); dam lake on Blue Nile in Sennar, 21. & 22.xi.2008, 8.ii.2010—nine spec. from Sud 372 (62974), 380 (62906), 392 (76421), 765 (IPCAS C-512), 779 (no voucher), 785 (IPCAS C-512) & 789 (no voucher); dam lake on the Atbarah River in Khashm el-Girba, 25. & 27.xi.2008—nine spec. from Sud 515 (62988), 522 (62989), 576 (76272), 580 (67089) & 582 (63142); Synodontis caudovittata Boulenger, 1901: White Nile in Kostí, 18. & 20.xi.2008—ten spec. from Sud 276 (62931), 280 (62932) & 342 (62943 & HWML 49528); Synodontis euptera Boulenger, 1901: Atbarah River in Khashm el- Girba, 27.xi.2008—one specimen from Sud 586 (63991); Synodontis frontosa Vaillant, 1895: Atbarah River in Khashm el- Girba, 25. & 26.xi.2008—15 spec. from Sud 533 (62990), 535 (62991), Sud 536 (no voucher), 544 (62992), 556 (77148) & 558 to 562 (62994 to 62997); Blue Nile in Sennar, 3. & 8. ii.2010—two spec. from Sud 758 (77149) & 778 (69934 & IPCAS C-512); Synodontis nigrita Valenciennes in Cuvier et Valenciennes, 1840: Blue Nile in Sennar, 23.xi.2008—two spec. from Sud 472 (62986); Atbarah River in Khashm el-Girba, 26.xi.2008—three spec. from Sud 559 & 560 (67090 & 62995); Synodontis serrata Rüppell, 1829: White Nile in Kostí, 1.ii.2010—two spec. from Sud 629 (70056) & 671 (69932); one specimen, from the dam on Blue Nile in Sennar, 8.2.2010; Synodontis sp. (probably S. schall): Khartoum, 22.3. 2006—one spec. from Sud 54 (50012); White Nile in Kostí, 26.iii. 2006—one spec. from Sud 125 (50026); Blue Nile in Sennar, 8.ii.2010—two spec. from Sud 793 (69933); Auchenoglanis cf. acuticeps: Blue Nile in Sennar, 21.xi.2008—one spec. from Sud 397 (62964). Turkana Lake Basin, Kenya. Synodontis schall: El-Molo Bay (Loiyangalani area), 17.xi.2006, 20.ix.2007, 25.ix.2008 & 31.viii.2009—30 spec. from T3/06 (MHNG INVE 69390), T4/06 (69392), T7/07 (77164), T35/07 (76387), T41/07 (62918), T57/07 (60792), T63/07 (69393), T322/08 (69766), T9/09 & 10/09 (76263, BMNH 2011.2.10.2–3, IPCAS C-512 & USNPC 104285); Longech village (by Kalokol), 29. 7 30.viii.2008—two spec. from T52/08 (69761) & T71/08 (69786); S. frontosa: El-Molo Bay, 21.ix.2008 and 2. & 3.ix.2009—five spec. from T256/08 (69763), T32/09 (70052) & T48/09 (70054 & 77175); Todonyang, 7.ix.2008—one spec. from T159/08 (69777); Longech village, 15.ix.2009—one spec. from T140/09 (70055).