Passerilepis zimbebel, Dimitrova & Georgiev & Mariaux & Vasileva, 2019

Dimitrova, Yana D., Georgiev, Boyko B., Mariaux, Jean & Vasileva, Gergana P., 2019, Two new cestode species of the family Hymenolepididae Perrier, 1897 (Cyclophyllidea) from passerine birds in Ethiopia, with the erection of Citrilolepis n. g., Syst Parasitol 96, pp. 279-297 : 280-286

Passerilepis zimbebel n. sp.

Type-host: Terpsiphone viridis ( Passeriformes : Monarchidae ), African paradise flycatcher.

Type-locality: Wondo Genet (7.08°N, 38.63°E), Ethiopia.

Type-material: A total of 14 specimens (coll. 23.xi.2012) and fragments of strobila (in total 21 slides. Holotype: MHNG-PLAT- 121392, a complete gravid specimen, stained and mounted in Canada balsam. Paratypes: MHNG-PLAT- 121393 (in total 16 slides), 7 specimens and fragments of strobila, stained whole-mounts; one slide with a scolex mounted in Berlese’s medium; IBER-BAS-C0159.1.1–1.3 (3 slides), two specimens, stained whole-mounts; one scolex in Berlese’s medium. Hologenophore (paratype): MHNG-PLAT- 121394, stained whole-mount.

Site in host: Small intestine.

Prevalence and intensity: 14 individuals; in 1 out of 1 bird studied.

Representative DNA sequence: cox 1 mtDNA, one sequence (GenBank: MK463854 ).

Etymology: The species name is after the Amharic name of the host, zimbe-bel; it is a noun in apposition.

Description ( Figs. 1 , 2 )

[Based on 14 specimens.] Body long, slender, ribbonshaped, when fully-developed with maximum length 21–28 mm (26, n = 3); maximum width at pregravid proglottides, 446–641 (559, n = 14); width at gravid proglottides 366–624 (542, n = 18); width at mature proglottides 391–495 (424, n = 20). Strobila consisting of 191–228 (215, n = 3) proglottides: 95–102 (98, n = 3) juvenile; 33–41 (38, n = 3) premature; 17–24 (21, n = 3) mature; 32–47 (41, n = 3) postmature; 3–4 (3, n = 3) pregravid; 5–14 (10, n = 3) gravid. Fully developed strobila (before starting apolysis) may contain 3–5 (n = 3) sterile terminal proglottides. Scolex oval, with conically protruded anterior part; 96–148 (125, n = 14) long and 141–210 (180, n = 14) wide at middle of suckers ( Fig. 1A ). Suckers oval, unarmed, directed antero-laterally, with moderately developed musculature; diameter of suckers 59–92 (78, n = 50). Rhynchus thin-walled, forming short, conical apical protrusion anterior to crown of rostellar hooks when rostellum invaginated. Rostellum sac-like, retractile, 119–145 (127, n = 11) long, 42–77 (60, n = 11) wide at middle, thick-walled, with muscular apical enlargement; intensely-stained glandular cells and retractor muscles present within its cavity. Rostellar sheath elliptical, thick-walled, passing beyond level of posterior margins of suckers, 121–162 (139, n = 10) long and 62–96 (78, n = 11) wide at middle; intensely-stained glandular cells present in its cavity, more densely distributed near bottom. Rostellar hooks 10 in number, in single row; hooks diorchoid, with very long handle with tapering and slightly curved and flattened end, short sickle-shaped blade and well-developed guard, shorter that blade ( Fig. 1B ). Measurements of hooks: total length 37–38 (38, n = 10); length of blade 9–10 (9, n = 10); length of base 28–30 (29, n = 10); distance between tip of blade and tip of handle 9–11 (10, n = 10). Neck 77–119 (93, n = 10) wide. Proglottides with well-developed velum. Inner longitudinal muscle bundles numerous. Genital pores unilateral, dextral, opening at anterior half of lateral proglottis margin ( Fig. 1C, D , 2A, B ). Genital atrium surrounded by intensely stained glandular cells, funnel-shaped, thickwalled, 22–27 (24, n = 10) deep, 2–7 (4, n = 10) wide at base, 7–17 (13, n = 10) wide at orifice ( Fig. 2C ); atrium eversible in mature proglottides, sometimes forming short genital papilla. Genital ducts dorsal to dorsal and ventral poral osmoregulatory canals in majority of proglottides. In some proglottides, genital ducts passing between dorsal and ventral poral osmoregulatory canal; number of proglottides with genital ducts passing between osmoregulatory canals varying in different specimens between 1 and 13% of all proglottides with well-developed genital ducts (mean = 4%; n = 438). Dorsal canal 2–10 (5, n = 41) wide, ventral canal 7–25 (13, n = 37) wide ( Fig. 2C ); no transverse anastomoses of both dorsal and ventral canals.

Strobila protandrous with gradual maturation. Testes 3, oval, with diameter 67–96 (83, n = 32), dorsal to female glands; situated in triangle, 2 antiporal and 1 poral to primordia of female gonads ( Fig. 1C, D , 2A ); their degeneration starting at postmature proglottides. External seminal vesicle elongate-oval, situated near to anterior proglottis margin, dorsal to female glands and antero-dorsal to seminal receptacle; connecting to cirrus-sac by distinct canal, 49–59 (53, n = 5) long and 7–17 (11, n = 11) wide in mature proglottides ( Fig. 2C ). Cirrus-sac lemon-shaped, thin-walled, 91–136 (117, n = 37) long, 45–62 (52, n = 37) wide, slightly oblique to anterior proglottis margin, crossing poral osmoregulatory canals, never reaching midline of proglottis ( Fig. 1D , 2 A–C). Ejaculatory duct surrounded by intenselystained cells. Internal seminal vesicle oval, occupying half of cirrus-sac when fully-developed, 49–94 (71, n = 41) long, 42–57 (47, n = 41) wide, surrounded by intensely stained glandular cells. Evaginated cirrus not available in material studied; armament in ductus cirri not observed ( Fig. 2C ).

Ovary with maximum width 161–222 (186, n = 10), median, ventral to testes and genital ducts, consisting of 3 compact lobes with oval or irregular shape ( Fig. 1D ). Vitellarium compact, sometimes with lobed margins, posterior and dorsal to ovary, ventral to testes and Mehlis’ gland; 62–106 (78, n = 15) wide, 32–57 (40, n = 15) long ( Fig. 1D ). Seminal receptacle thin-

walled, voluminous, 87–168 (128, n = 18) long, 57–101 (80, n = 18) wide, posterior and ventral to cirrus-sac and external seminal vesicle, dorsal to ovary and uterus, connected with oötype by distinct duct, 24–29 (27, n = 5) long, 10–12 (12, n = 5) wide ( Fig. 2A ). Vagina opening ventrally to cirrus-sac, usually passing laterally and sometimes posteriorly to it, surrounded by thick sleeve of intensely stained cells. Vagina consisting of well-defined copulatory part and conductive part; copulatory part tubular, 62–99 (79, n = 30) long, 7–23 (12, n = 34) wide, with thick walls consisting of strong circular musculature; conductive part thin, tubular, 10–17 (13, n = 13) long, 2–5 (3, n = 13) wide ( Fig. 2C ).

Young uterus appearing as thick-walled, transversely-elongate narrow sac, with ends slightly curved in posterior direction; situated in median field, anterior to vitellarium, dorsal to ovary and ventral to seminal receptacle, Mehlis’ gland and testes ( Fig. 1D ), not crossing lateral osmoregulatory canals; uterine walls containing large intensely stained cells. With further development, uterus enlarging laterally but its middle part remaining slightly narrower than lateral parts in postmature proglottides ( Fig. 2A ). Gravid uterus sacciform, filling entire median field of proglottis, slightly overlapping but not crossing lateral osmoregulatory canals ( Fig. 2B ). Eggs 42–67 (52, n = 25) in diameter, with thin outer coat; embryophore elliptical, thickwalled, 35–47 (40, n = 25) long, 32–37 (35, n = 14) wide, with thickness of walls 2–7 (3, n = 30); no polar filaments observed on embryophore; oncosphere elliptical, 29–37 (33, n = 30) long and 22–27 (25, n = 14) wide. Embryonic hooks differing in shape and length: median pair 20–21 (20, n = 13) long; internal lateral pair more robust, 17 (17, n = 26) long; external lateral pair 16–17 (17, n = 26) long ( Fig. 2D ).

Remarks

The present material corresponds to the original diagnosis of the genus Passerilepis as defined by Spasskii & Spasskaya (1954). The specimens from Terpsiphone viridis are characterised by a rostellum armed with a single row of ten hooks, the diorchoid shape of the rostellar hooks (with a long handle, shorter blade and small but well-developed guard), unarmed suckers, three testes situated in a triangle (one poral and two antiporal), the cirrus-sac not reaching the midline of the proglottis, the absence of accessory sacs in the genital atrium, the median female gonads and the sacciform uterus. Initially, the genus Passerilepis incorporated fifteen cestode species parasitising mainly passerine birds ( Spasskii & Spasskaya, 1954). The analysis of the previous records revealed 23 valid species of this genus parasitising mostly terrestrial birds of the orders Passeriformes , Coraciiformes and Trogoniformes in the Holarctic, Neotropical, Nearctic, Afrotropical and Oriental Regions ( Spasskii & Spasskaya, 1954, 1964; Yamaguti, 1956, 1959; Spasskaya, 1966; Schmidt, 1986) (see Table 1).

The most frequently used characters for the identification of Passerilepis spp. are the length and the shape of the rostellar hooks ( Spasskii & Spasskaya, 1954, 1964). The specimens of the present material possess rostellar hooks 37–38 µm long, thus resembling four described species of Passerilepis having rostellar hook with lengths 34–40 µm ( Table 1). These are P. septemsororum ( Burt, 1944) , P. dahurica ( von Linstow, 1903) , P. pellucida ( Fuhrmann, 1906) and P. brevis ( Fuhrmann, 1906) . According to the classification of the rostellar hooks of hymenolepidids from birds ( Skrjabin & Mathevosian, 1945), two of these species ( P. dahurica and P. brevis ) are characterised with arcuatoid type of hooks, i.e. a hook with a long handle, a weakly-developed small blade and a guard almost as long as the blade (see also the definition in Khalil et al., 1994). In contrast, the specimens from Ethiopia are characterised by the diorchoid shape of the hooks. The hooks of P. pellucida have a longer blade compared to the arcuatoid type of hooks of the above-mentioned species. However, its guard is thicker, and the shape of this hook is rather fraternoid (Fuhrmann, 1906a). The hooks of P. septemsororum have an intermediate shape between diorchoid and arcuatoid, i.e. with a very long handle and much shorter claw-like blade, the guard is prominent and thick ( Burt, 1944).

The specimens from Ethiopia can also be distinguished from the remaining valid Passerilepis spp. by some features of the strobilar morphology, i.e. the position of the genital ducts in relation to the osmoregulatory canals and the shape of the female gonads. Similarly to the majority of the avian hymenolepidids ( Czaplinski & Vaucher, 1994), the species of Passerilepis have genital ducts passing dorsally to the poral osmoregulatory canals and this character remains constant in all proglottides of the strobila. The majority of the studied specimens from T. viridis have strobila consisting of proglottides with the same position of the genital ducts. There are exceptions in several specimens where the genital ducts pass between the dorsal and ventral poral osmoregulatory canals (in 4% of proglottides on average). This variation in the position of the genital ducts has not been observed in other Passerilepis spp. Since the frequency of occurrence of this configuration is not high, we think it can be considered as anomalous. The specimens from Ethiopia are also characterised by a median ovary consisting of three compact lobes of oval or irregular shape as well as by the compact median vitellarium. In contrast, the female gonads of P. stylosa (Rudolphi, 1809) and P. crenata (Goeze, 1782) are multilobate.

Four species of Passerilepis have been recorded in the Afrotropical Region. These are P. stylosa , P. passeris (Gmelin, 1790) , P. passerina ( Fuhrmann, 1907) and P. crenata . Passerilepis passerina is known only from its original description from ‘‘ Turdus parochus ’’ (most probably, a mislabelled sample, see Kuchta et al., 2012) from Egypt ( Fuhrmann, 1907). It differs from the present specimens from Ethiopia by its arcuatoid hooks (see figure 30 in Fuhrmann, 1907) which are of considerably smaller size (20 vs 37–38 µm in specimens from Wondo Genet). In addition, the cirrus-sac in P. passerina is much longer, i.e. 200 vs 91–136 µm in P. zimbebel n. sp. The remaining three species, i.e. P. passeris , P. stylosa and P. crenata , are among the most frequently recorded Passerilepis spp. worldwide. The only Afrotropical record of P. passeris is from Dicrurus modestus Hartlaub (Dicruridae) from the Democratic Republic of the Congo ( Southwell & Lake, 1939). Passerilepis passeris is characterised by its almost diorchoid hooks but they are considerably shorter than the hooks of P. zimbebel n. sp. ( Table 1). In addition, P. passeris has a multilobate ovary ( Spasskaya, 1966), whereas the ovary of the new species has three almost oval and compact lobes. The African record of P. crenata is from Corvus cornix (L.) ( Corvidae ) in Egypt ( Krabbe, 1869). This species differs significantly from our material by its rostellar hooks, which are 20–26 µm long and their shape is similar to fraternoid. The African record of P. stylosa is from Baeopogon indicator (Verreaux & Verreaux) (Pycnonotidae) from the Democratic Republic of the Congo ( Southwell & Lake, 1939). This species differs from the specimens from Ethiopia by the arcuatoid shape of its hooks. As was mentioned above, P. stylosa differs from the specimens from Ethiopia by its multilobate ovary.

The specimens studied differ from the remaining Passerilepis spp. by the length of the rostellar hooks ( Table 1).

Based on the above-mentioned differences, we recognise the specimens from Terpsiphone viridis in Ethiopia as a new species, P. zimbebel n. sp.

Figures

Fig. 1 Passerilepis zimbebel n. sp. A, Scolex; B, Rostellar hooks in various positions (first two hooks in lateral position); C, Male mature proglottis; D, Hermaphroditic mature proglottis with an early stage of uterine development. Scale-bars: A, 50 µm; B, 30 µm; C, D, 100 µm

Fig. 2 Passerilepis zimbebel n. sp. A, Postmature proglottis; B, Gravid proglottis; C, Genital ducts in a mature proglottis, dorsal view; D, Egg. Scale-bars: A–C, 100 µm; D, 50 µm