Revue suisse de Zoologie 114 (1): 141-174; mars 2007 Cestodes ofthe genus Biuterina Fuhrmann, 1902 (Cyclophyllidea: Paruterinidae) from passeriform and piciform birds in the Ivory Coast, with a key to the species ofthe genus Boyko B. GEORGIEV1-2 & Jean MARIAUX3 1Central Laboratory ofGeneral Ecology, BulgarianAcademy ofSciences, 2 Gagarin Street, 1113 Sofia, Bulgaria. E-mail: [email protected] 2Department ofZoology, Natural History Museum, Cromwell Road, London SW7 5BD, UK. 3Natural History Museum, RO. Box 6434, 1211 Geneva 6, Switzerland. E-mail: [email protected] Cestodes of the genus Biuterina Fuhrmann, 1902 (Cyclophyllidea: Paruterinidae) from passeriformand piciformbirdsintheIvory Coast, with a key to the species ofthe genus.- On the basis ofrecently collected material fromthe Ivory Coast (République de Côte d'Ivoire) and other spe- cimens fromthe collections ofGenevaNatural History Museum,we review the species of Biuterina (Paruterinidae) known from that country. Five species are recorded, among which two are new: B. pogoniuli sp. n. from Pogoniulus scolopaceus (Piciformes: Capitonidae) and B. petroniae sp. n. & from Petronia dentata (Paseriformes: Ploceidae). B. africana Joyeux Baer, 1928, from Tchagra spp. (Passeriformes: Laniidae), is redescribed on the basis of the type material from Benin, as well as of specimens from Angola, Guinea and the Ivory Coast. The species is reported for the first time from the latter two countries. B. pentamyzos (Mettrick, 1960) from Prionopspiumata in Zimbabwe is recognised as a synonym ofB. africana (new synonymy). B. cordifera Murai & Sulgostowska, 1983 and B. trian- gula (Krabbe, 1869) are reported from new hosts (Acrocephalus arundi- naceus andAnthus leucophrysgouldii,respectively) andforthe firsttime in Africa. An identification key to the 34 species of Biuterina presently recognized worldwide is given. Keywords: Parasite - helminths - Paruterinidae - Biuterina - Africa - Ivory Coast - systematics - morphology - Laniidae - Ploceidae - Capitonidae - Sylviidae - Motacillidae. INTRODUCTION Biuterina Fuhrmann, 1902 comprises cestode parasites from passeriform and coraciiform birds; the number ofthe included species is considered to be between 30 and 40 depending on the generic definition adopted or on the views on the species validity (Matevosyan, 1969; Bona & Maffi, 1984; Schmidt, 1986; Kornyushin, 1989; Manuscriptaccepted 12.12.2006 142 B.B.GEORGIEV & J. MARIAUX Mariaux & Vaucher, 1989; Georgiev & Kornyushin, 1994; Georgiev et al., 2002, 2004). The species diversity ofthis genus is relatively well studied in temperate lati- tudes (e.g., Matevosyan, 1969; Kornyushin, 1989; Georgiev et al., 2004). However, mostofthe tropicalBiuterina spp. areknown from single records only. Five ofthe six species originally described from Afrotropical birds were recently redescribed & (Mariaux Vaucher, 1989; Georgiev etal., 2002), but data on their geographical dis- tributionandhostrangesremainedscarce.Theonlyextensivefaunisticsurveyonavian cestode inAfrica during the last 20 years was carried out in the Ivory Coast (for sum- marised data, see Mariaux, 1994); however, some ofthe paruterinid species remained identified only at the generic level and their detailed taxonomic description required additional studies. The aim of the present article is to report new data on the morphology and taxonomy of Biuterina spp. collected from birds in the Ivory Coast, West Africa. In addition, we provide an identification key to the species ofthe genus. MATERIALAND METHODS In total, 1,252 birds belonging to 174 species, 104 genera and 39 families were studied in the Ivory Coast by one of the present authors (JM) during 1985-1988 (for more detailed data, see Mariaux, 1994). Birds were captured with mist nets or shot. They were dissected immediately after death. Cestodes were removed from guts and fixedin 5% hotformalin.They were stored in 70% ethanol, stained in alcoholic hydro- chloric carmine, dehydrated in ethanol series, cleared in clove oil and mounted in Canada balsam. Some scoleces were mounted in Berlese's medium to facilitate the examination ofthe rostellar hooks. The specimens were deposited in the Invertebrate Collection of the Natural History Museum, Geneva (MHNG). Details on their collection data and number ofspecimens are given in the text foreach species. The metrical and meristic data are presented as the range, with the mean in parentheses and the number ofmeasurements or counts taken (n). The measurements are given in micrometres unless otherwise stated. The developmental stages of the proglottides are designated as previously described (Georgiev & Vaucher, 2001). The nomenclature forthe birds follows Howard & Moore (1980). TAXONOMIC PART Biuterina africana Joyeux & Baer, 1928 ParuterinapentamyzosMettrick, 1960,new synonymy Biuterinapentamyzos (Mettrick, 1960) Matevosyan, 1964 Material examined: MHNG INVE 44454-44455 (Collection Joyeux, nos CJ 28/73a and CJ 28/74a), 2 slides, labelled "Biuterina africana, Telephonus senegalus, Gendre", one of them containing a stained scolex squashed in Canada balsam, and the other containing three stainedpregravid specimens inCanadabalsam; recognisedhere as syntypes ofB.africana (see Remarks); from Tchagra senegala (synonyms Pomatorhynchus senegalus, Telephonus sene- galus) (Passeriformes: Laniidae) collectedatBohicon,BeninbyE.Gendre (seeJoyeux&Baer, 1928); substantial parts of strobila contracted. -MHNG INVE 44456 (Collection Joyeux, nos CJ 28/75aandCJ 28/78),2 slides,labelled"Biuterina africana, Telephonussenegalus,Gendre, Labe",containinglongitudinalsectionsofstrobilarfragmentsofmatureandpostmatureproglot- tides;from TchagrasenegalacollectedatLabe,GuineabyE.Gendre;thesespecimenswerenot mentioned in the publications ofJoyeux. - MHNG INVE40301 (Collection Fuhrmann - Baer , BIUTERINA SPP. FROM THE IVORYCOAST 143 nos 20/60-63), 4 slides, labelled "Biuterina africana, pie grièche, Angola" (two slides) or "Biuterina africana, Pomatorhynchus, Angola" (2 slides); mentioned by Fuhrmann (1943). Exact host names are not given in the labels; according to Fuhrmann (1943), B. africana was recorded in Angola from Pomatorhynchus australis (Smith) [now Tchagra australis (Smith)] Pomatorhynchus senegalus (L.) [now Tchagra senegala (L.)] and Pomatorhynchus anchietae (Bogage) [now Tchagraminutaanchietae(Bocage)] (Passeriformes,Laniidae).-MHNGINVE 16117 (former no 988.414, see Mariaux, 1994), 4 slides (2 fragmented specimens stained in hydrochloric carmine and mounted in Canada balsam and 2 scoleces mounted in Berlese's medium), from Tchagra senegala pallida (Neumann) (Passeriformes: Laniidae), collected at Tortyia, Ivory Coast, on 10 February 1987, by J. Mariaux; mentioned by Mariaux (1994). The hostspecimenhasbeendepositedintheOrnithologicalCollectionoftheMHNG,no. 1768.047. Re-description of the syntypes: Pregravid specimens with band-like body, 11.2-14.2 mm (12.4 mm, n =3) long, consisting of 106-114 (109, n=3) proglottides; contracted, single specimen with relaxed portions ofstrobila; maximum width at pre- gravid proglottides, 612-734 (654, n = 3). Scolex wider than neck, laterally rounded, withmaximumwidth atmiddleofsuckers,385-450 (420,n= 3) (Fig. 1). Suckersoval, 115-130 (121, n = 7) in diameter, with well-developed musculature; in single spe- cimen, inner surface of suckers with punctiform spines (not distinct in remaining specimens). Rostellum sucker-like,retracted in all available specimens, with diameter 125-145 (133, n = 3); vertical muscular fibres inside distinct. Thick layer of radial muscular fibres surround rostellum (Fig. 1); glandular cells surround radial muscu- lature. Rostellar hooks arranged in 2 regular rows; 2 of4 available scoleces had mis- sing rostellar hooks and others had densely packed hooks, for which exact number is difficult to determine but there are at least 38. Each hook with epiphyseal thickening on both handle and guard. Anterior hooks 75-80 (78, n = 12) long; blade longer than handle (Fig. 2). Posterior hooks 55-60 (58, n = 12) long; blade shorter than handle (Fig. 3). Rostellar hooks with blades directed anteriorly when rostellum is retracted. Genital pores irregularly alternating in short series,e.g. ... 2, 1,3, 1,2, 1,2,5, 1,2,2, 2; pores open about middle oflateral proglottis margin. Genital atrium represented by infundibular distal part with thick walls and tubular proximal part surrounded by aggregation ofglandular cells (Fig. 5). Dorsal osmoregulatory canals 5-8 (n = 10) in diameter; ventral osmoregulatory canals with diameter 13-38 (n= 10),with transverse anastomoses along posteriorproglottis margin. Genital ducts pass between osmoregu- latory canals. Testes 10-14(11,n= 15)innumber,oval,formcompactgroupinposteriormost partofmedian field,posterior,dorsal andlateral tovitellariumandposteriorandlateral to ovary, may overlap posterior margins of ovary dorsally (Fig. 4). External vas deferens coiled, with diameter 5-8 (7,n = 10), forms dense body in anteriorporal part ofmedian field together with surrounding glandular cells. Cirrus-sac highly elongate, 193-225 x 27-41 (215 x 33, n = 10), mostly cylindrical, tapered porally and rounded antiporally, thick-walled, usually crosses poral osmoregulatory canals. Internal vas deferenscoiled.Evaginatedcirrus notobserved; minute (>1 piralong) triangularspines present in canal ofwithdrawn cirrus. Ovary 110-145 (122, n = 10) wide, symmetrical, consisting of 2 compact rounded wings. Vitellarium compact, oval, 42-60 (52, n = 10) in diameter, at some distance from posterior proglottis margin (Fig. 4). Mehlis' gland indistinct. Seminal receptacle elongate, situated dorsally, mostly between wings of ovary, extends from 144 B. B. GEORGIEV & J. MARIAUX Figs 1-3 BiuterinaafricanaJoyeux & Baer, 1928,syntypes from Tchagrasenegala inBenin. (1) Scolex. (2)Anteriorrostellarhooks. (3) Posteriorrostellarhooks. Scalebars: 1, 100/<m; 2,3,50jim. poral part ofmedian field at level anterior to ovary to level ofvitellarium, 105-118 x 28-33 (112 x 30, n = 7). Vagina opens postero-laterally to male pore, with copulatory part 138-180 (169,n = 7) long and 18-23 (20,n= 10) indiameter,consistingofthick- walled vaginal canal and cellular sleeve along entire length, with diameter of lumen 4-7 (6, n = 7), wider at poral end; conductive part ofvagina short, narrow. Uterus inmatureproglottides sac-like,sphericalorwith slightlyirregularshape, thick-walled (Fig.4). Primordium ofparuterine organ appears as consolidation ofcen- tral part ofmedullary parenchyma anterior to uterus. In pregravid proglottides, uterus consists of2 sacs connected by transverse isthmus; paruterine organ elongate, may be slightly convoluted, with tapering anterior end surrounded by granular tissue (Fig. 6). No fully-developed eggs in specimens available. Description of the material from the Ivory Coast: Strobila band-like, gradually widening in posterior direction, with maximum width 751-848 (n = 2) at level ofpregravidproglottides. Scolexrounded, widerthanneck, with conical anterior protrusion (Fig. 7); maximumwidth 372-437, atmiddle ofsuckers. Suckers oval, 130- 161 (144,n= 8) indiameter, withdevelopedmusculature; theirinnersurfaceprovided punctiform spine-like structures intransverserows (Fig. 7, 12). Rostellum sucker-like, BIUTERINASPP. FROM THE IVORYCOAST 145 Figs 4-6 BiuterinaafricanaJoyeux & Baer, 1928,syntypes from Tchagrasenegala inBenin. (4) Mature proglottis,dorsalview.(5) Genitalducts inamatureproglottis,dorsal view. (6)Gravidproglot- tis. Scalebars: 4,6,200firn; 5,50//m. with diameter 148 (n = 1) when retracted and 186 (n = 1) when protruded. Rostellum surrounded by thick layer ofradial muscular fibres and intensely staining glandular cells (Fig. 7). Rostellum armed with 38 (n = 3) or42 (n = 1) rostellar hooks arranged in2 regularrows. Each hookprovidedwith epiphyseal thickening on both handle and guard. Anteriorhooks 82-85 (83, n = 6) long, with length ofrefractive particle 81-82; 146 B.B. GEORGIEV & J. MARIAUX blade longer than handle (Fig. 8). Posterior hooks 61-63 (62, n = 6) long, with length ofrefractiveparticle 58-60; blade shorterthanhandle (Fig. 9). Proglottides craspedote; mature proglottides wider than long (Fig. 10); gravidproglottides slightly longerthan wide (Fig. 11). Genital pores irregularly alternating in short series, open about middle oflateralproglottismargin. Genitalatriumconsistsofinfundibularthick-walledorifice andtubularhermaphroditic canal surroundedby intensely staining cells. Dorsal osmo- regulatory canals 4-8 (n = 10) in diameter. Ventral osmoregulatory canals with diameter 22-47 (n = 10), with transverse anastomoses along posterior margin ofeach proglottis. Genital ducts betweenporal osmoregulatory canals. Testes 10-15 (12, n = 11) in number, oval, situated in compact group posterior, dorsal and lateral to vitellarium and posterior and lateral to ovary, may overlap posterior margins ofovary (Fig. 10). External vas deferens coiled, with diameter 5-12 (7, n = 10), together with surrounding intensely stained cells forming dense body in anteriorporal partofmedian field. Cirrus-sac highly elongate, 171-232 x 30-37 (201 x 34, n = 10), mostly cylindrical, with tapering poral end and rounded antiporal end, thick-walled; in mature proglottides, usually cross poral osmoregulatory canals; in gravid proglottides, often entirely situated in lateral field or slightly crossing poral osmoregulatory canals. Internal vas deferens coiled. Evaginated cirrus not observed; minute (length < 1 pirn) triangular spines with pointed tips seen in canal ofwithdrawn cirrus. Ovary consisting of2 compact symmetrical wings. Vitellarium compact, oval, 51-69 (62, n = 10) in diameter, at some distance from posterior proglottis margin (Fig. 10). Mehlis' gland not observed as glandular structure. Seminal receptacle elon- gate, situated mostly dorsally between wings of ovary, extends from poral part of median field at level anterior to ovary to level of vitellarium. Vagina opens postero- laterally to male orifice, with copulatory part 174-223 (193, n = 7) long, 14-23 (18, n = 10) in diameter, consisting of thick-walled vaginal canal and thick cellular sleeve along entire length; poral part of vaginal canal wider, covered with distinct micro- triches; conductive part ofvagina short and thin. Uterus in mature proglottides sac-like, spherical or with irregular shape, thick- walled (Fig. 10). Primordium of paruterine organ appears as consolidation ofcentral part ofmedullary parenchyma anteriorto uterus. In pregravid and gravid proglottides, uterus consists of2 sacs connected by thin transverse isthmus; paruterine organ elon- gate, with tapering anterior end surrounded by granular tissue (Fig. 11). Eggs oval; outerenvelopes thin,often not distinct. Embryophore oval,thick, with diameter40-45 (43, n = 10). Oncosphere oval, with diameter 28-34 (31, n = 10). Embryonic hooks: central pairs 19-21 (20, n = 7) long; lateral pairs 16-18 (17, n = 10) long. Remarks: Biuterina africana Joyeux & Baer, 1928 was described from & Tchagra senegala (L.) (Passerifomes, Laniidae) at Bohicon, Benin (Joyeux Baer, 1928). Subsequently, it was recorded from the type host inAngola (Fuhrmann, 1943) and the Ivory Coast (Mariaux, 1994), and also from two other species of Tchagra Lesson, T. minuta (Hartlaub) and T. australis, inAngola (Fuhrmann, 1943). The only information on its morphology is the brieforiginal description (Joyeux & Baer, 1928). We found substantial differences between the material from the Ivory Coast and the original description inrelation to the size ofthe rosteliarhooks. Othercharacters were BIUTERINA SPP. FROMTHEIVORYCOAST 147 Figs 7-9 BiuterinaafricanaJoyeux&Baer, 1928,materialfromtheIvoryCoast.(7) Scolex. (8)Anterior rostellarhooks. (9) Posteriorrostellarhooks. Scalebars: 7, 100pirn; 8,9,50pim. difficultto compare because the original description is illustrated with drawings ofthe scolex and rostellar hooks only; few strobilar characters are described and none of them illustrated.This provoked the presentredescription ofthe type material. None ofthe specimens ofB. africana in the Collection ofC. Joyeux (currently deposited in the MHNG) is indicated as type material. We examined 4 slides from the MHNG type host «Telephonus senegalus» and recognised as syntypes two slides, 148 B. B. GEORGIEV & J. MARIAUX Figs 10-11 BiuterinaafricanaJoyeux&Baer, 1928,materialfromtheIvoryCoast.(10).Matureproglottis, dorsal view. (11) Gravidproglottis. Scalebars: 10, 100^m; 11,200^m. MHNG 44454and 44455 (CollectionJoyeuxnosCJ28/73aandCJ28/74a),sincethen- labels areconcordantwiththeinformationincludedinthepapercontainingtheoriginal description (Joyeux & Baer, 1928). The other two slides of B. africana in Joyeux' MHNG collection, 44456 (Collection Joyeux nos CJ 28/75a and CJ 28/78), contain BIUTERINA SPP. FROMTHE IVORYCOAST 149 sectioned strobilar fragments of the same species; however, according to the labels, they were collected at Labe (Guinea) and therefore do not belong to the type series. Our study revealed discrepancies in the original description in relation to the length of the posterior rostellar hooks and the number of the testes (Table 1). In addition, we found that the most developed specimens of the type series were pregravid; therefore,the original measurements ofthe body length andthe diameterof the eggs are not reliable.The material from the Ivory Coast corresponds well with the morphology ofthe type series; some differences in the measurements ofthe rostellum and suckers are probably due to the different state of the material (rather contracted type specimens versus relaxed specimens from the Ivory Coast). We confirm the identification of Fuhrmann's (1943) material from Angola, although we are not sure ofthe identity ofthe host species ofthe available specimens. Their morphology corresponds well with that of the type series, including to the respective metrical and meristic data (Table 1). The new morphological data on B. africana enables a re-evaluation of the validity ofanotherAfrotropical species ofBiuterina,B.pentamyzos (Mettrick, 1960), a parasite of Prionops piumata poliocephala Shaw (Passeriformes, Laniidae) in Zimbabwe (Mettrick, 1960). Its type material was recently redescribed (Georgiev et al., 2002). The morphology ofthe scolex and both mature and uterine proglottides of B. pentamyzos entirely corresponds to the present redescription of B. africana, including the metrical data (Table 1). The difference in the body dimensions is due to taking measurements from afully-developed (gravid) and well-relaxed specimenfrom the type series ofB.pentamyzos (see Georgiev etal., 2002) compared with the rather contractedandnotfully-developed syntypesofB.africana.Therefore,werecogniseB. pentamyzos as ajunior synonym ofB. africana. Georgiev etal. (2002) reportedthepresenceofan armatureontheinnersurface ofthe suckers ofB.pentamyzosconsistingof"fine,punctiform,spine-like structures in transverse rows". This is distinct in the material from the Ivory Coast (Fig. 12). However, it is hardly seen in one ofthe syntypes ofB. africana and not distinct in the remaining specimens, probably because of the contracted condition of the scoleces resulting in a highly folded internal surface ofsuckers. Matevosyan (1969) mentioned Tunisia as the only locality for B. africana. However, we did not find any published record of the species from that country. Summarising the above data, the geographical range ofB. africana includes Guinea, theIvoryCoast,Benin (typelocality),AngolaandZimbabwe; itshosts arerestrictedto birds ofthe family Laniidae: Tchagra senegala (type host), T. australis, T. minuta and Prionopspiumata. Biuterina cordifera Murai & Sulgostowska, 1983 Materialexamined: MHNG INVE 15927 (formerly no. 987.273, see Mariaux, 1994), 1 slide(fragmentsof2specimens), 14January 1987,hostcollectionnumberCI440andMHNG INVE 15928 (formerlyno.987.274,seeMariaux, 1994), 1 slide (fragmentsof2 specimens), 15 January 1987, host collection number CI 447, from Acrocephalus arundinaceus (L.) (Passeriformes, Sylviidae),collected atAdiopodoumé. One ofthe host specimens (CI 447) has beendeposited in the Ornithological Collectionofthe MHNG,no. 1769.041. Description: Strobilagradually widening posteriorly; maximum width at level ofgravidproglottides 559-578 (n =2). Scolex (Fig. 13) rounded,withmaximumwidth 150 B. B. GEORGIEV & J. 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