Raillietina hymenolepidoides, Mariaux & Georgiev, 2020

Mariaux, Jean & Georgiev, Boyko B., 2020, Cestode parasites (Neodermata, Platyhelminthes) from Malaysian birds, with description of five new species, European Journal of Taxonomy 616, pp. 1-35 : 17-21

Raillietina hymenolepidoides sp. nov.

urn:lsid:zoobank.org:act:0E5860D5-3EAA-4F26-8F0D-DF5ED3718219

Figs 22–26 , Table 2

Etymology

The species name refers to the overall similarity of the strobilar anatomy of this species to that of cestodes of the family Hymenolepididae .

Material examined

Holotype

MALAYSIA • Selangor, University of Malaya’s Gombak Field Station ; 3.32° N, 101.77° E; 280–350 m a.s.l.; 1 Aug. 2010; MHNG-PLAT-120869.

Paratypes

MALAYSIA • 2 specs; same collection data as for holotype; MHNG-PLAT- 120870 .

Hologenophore

MHNG-PLAT- 120869. Partial COI sequence, Genbank MN590290 . Additional sequence: MHNG- PLAT-130033. Partial COI sequence, Genbank MN590289 .

Comparative material

PHILLIPINES • holotype and two paratypes of Raillietina palawanensis Deardorff, Schmidt & Kuntz, 1976 from Chalcophaps indica (Linnaeus, 1758) ( Columbiformes , Columbidae ); Palawan Island ; May– Jun. 1962; NHM 1369066, 1369067 .

Type host

Chalcophaps indica (Linnaeus, 1758) ( Columbiformes , Columbidae ).

Prevalence

50% (2/4).

Description

Body very thin and fragile, of medium size; maximum length 55 mm, width mostly 150–350 along entire length of worm, reaching maximum of 425 at level of gravid proglottides; consisting of up to 800 proglottides. Proglottides craspedote, always wider than long except for very last gravid ones; detached gravid proglottides may be almost spherical. Scolex very small, well-delineated from neck, 100–137 (122, n = 3) in diameter. Suckers rounded, 34–43 (39.5, n = 10) in diameter, muscular, armed with 4–5 dense rows of hooklets, 6–8 in length ( Fig. 22b ). Rostellar sac absent. Rostellum discoid, 46–69 (61, n = 3) in diameter, muscular, armed with double row of 150–160 small typical davaineid hooks of length 7–8 ( Figs 22a, 23 ). Pseudoproboscis armed with clearly visible minute accessory spines on about 50 of length ( Fig. 22c ). Neck well-marked, narrow, 50 in diameter; followed by a long unsegmented section. Proglottization distinct at about 2.5 mm from posterior margin of suckers. Genital pores unilateral, situated slightly anteriorly to mid-length of lateral proglottis margin. Ventral osmoregulatory canals up to 40 wide, connected posteriorly in each proglottis by transverse anastomosis. Dorsal osmoregulatory canals absent. Genital ducts dorsal to ventral osmoregulatory canals. Genital atrium small, 7–13 × 9–21 (9 × 14, n = 21), infundibular, with wide orifice.

Testes 3 in number; most commonly in triangle, 2 posterior and 1 anterior antiporal, but with frequent variations, sometimes more or less in posterior line, partially overlapping each other ( Fig. 24 ); slightly oval, 35–50 in maximal diameter (43, n = 33). External vas deferens short and making only few coils antero-laterally to proximal end of cirrus-sac. Cirrus-sac elongate, 63–81 × 28–39 (74 × 34, n = 22), straight, with strong wall, reaching osmoregulatory canals, rarely crossing them ( Fig. 25 ); proximal extremity of cirrus-sac often directed anteriorly, positioning cirrus-sac almost parallel to proglottis lateral margin. Internal vas deferens forming a few coils and distinctive proximal dilatation resembling internal seminal vesicle. Cirrus armed with dense long setae.

Vitellarium posterior, central, compact, 26–35 × 17–26 (30 × 21, n = 14). Ovary antero-central, transversely elongate, bilobed, compact and becoming massive, dumbbell-shaped. Mehlis’ gland anterior to vitellarium. Vagina opens posterior to male pore, copulatory part 25–48 × 6–15 (36 × 12, n = 15), with strong walls, surrounded by a large but discrete muscular sphincter ( Fig. 25 ). Proximal (conductive) part of vagina straight, thin, without cellular sleeve, with length similar to that of copulatory part; parallel to posterior wall of cirrus sac; connected with seminal receptacle in lateral field of proglottis. Seminal receptacle slightly convoluted, tubular, crossing poral osmoregulatory canal, poral to ovary.

Uterus starts its development in late mature proglottides as a small antero-dorsal and central sac; with further development, turning into transverse sac filled with large developing eggs; confined in median field. Uterus eventually forming 8–12 (10, n = 13) egg capsules situated in 2 layers, each one containing 5– 10 eggs (7, n = 30) ( Fig. 26 ), occasionally overlapping excretory canals. Eggs often, but not always, developing at different rates, possibly leading to the simultaneous presence of fully developed eggs together with others at diverse stages of development within a single capsule. Eggs globular, 32–39.5 (36.5, n = 27). Oncospheres round to oval, 12–14 (13, n = 20) along longest axis. Embryonic hooks subequal, 5.5–7 (6, n = 12) in length.

Remarks

Columbiformes are second only to Galliformes as hosts for cestodes of the genus Raillietina . Over 60 species of these worms have been reported from pigeons and doves ( Movsessian 2003a), three of them in Malaysia ( Amin-Babjee & Lee 1992; Lee et al. 1998). In addition, R. palawanensis Deardorff, Schmidt & Kuntz, 1976 was described by Deardorff et al. (1976) in C. indica in the Philippines. To our knowledge, no other species have subsequently been described from these hosts.

Our material is quite unique in having an extremely reduced and constant number of testes per proglottis and can thus easily be differentiated from all these taxa. Although the number of testes is very variable among species of Raillietina , only a very few have fewer than 5, and none has 3 as observed in our specimens. Two species, R. palawanensis and R. quadritesticulata Moghe, 1925 , are nevertheless relatively similar, though not identical, to our material for this character (3–4 and 4 testes, respectively, according to their descriptions). We reexamined part of the R. palawanensis type series, including its holotype, and although several original observations in Deardorff et al. (1976) are confirmed, we also observed several significant differences ( Table 2 ):

– the worms are much longer (length more than 60 mm, complete specimen probably more than 100 mm long) and wider (up to 790 at level of gravid proglottides);

– the dorsal osmoregulatory canals are absent (likely mistaken for longitudinal muscle bundles in the original description);

– testis number is essentially 4 (5 is not unusual, 3 and 6 are very rare); it should be noted that the initial development of testes is not synchronous, with one, sometimes two, antiporal testes showing a delayed growth;

– the cirrus sac may be slightly larger than reported (up to 120 in length and 56 in width);

– the copulatory vagina part is longer (39–52);

– up to 17 egg capsules per proglottis, each containing up to 7 eggs can be observed in gravid proglottides;

– oncospheres are 16–18 in diameter.

These observations confirm that R. palawanensis differs from our material by having a larger scolex and rostellum and fewer, much larger, rostellar hooks, as well as a larger cirrus-sac, while R. quadritesticulata has more rostellar hooks, a larger cirrus-sac and more egg-capsules per proglottis ( Table 2 ). Our material is therefore clearly distinct and we place it in a new species, Raillietina hymenolepidoides sp. nov.

Interestingly, all three species with an extreme reduction of testis number are found in South/South East Asia and two in the same host species. Although this clearly suggests a close relationship between these taxa, the significance of this observation in a phylogenetic context remains to be studied. A similar reduction in testis number is observed in the genus Diorchiraillietina Yamaguti, 1959 , whose single species has only 2 testes per segment. It is found in various pangolin species in Africa and South Asia, including in species distributed in Malaysia, and may be indicative of a host-switching event. Molecular samples from pangolin parasites would allow the examination of this hypothesis.

The absence of dorsal excretory canals is an uncommon feature found in some davaineids. It is observed in the monotypic genera Porogynia Railliet & Henry, 1909 and Baerfainia Yamaguti, 1959 . The latter, found in African Pholidota and erected for Raillietina anoplocephaloides Baer & Fain, 1955 ( Yamaguti 1959) , shows a similar reduction of testis numbers (4, sometimes 3) as observed in our material. Its rudimentary rostellum and particular vagina structure are, however, very different.

Figures

Figs 22–26. Raillietina hymenolepidoides sp. nov. 22. a) Complete rostellar crown. b) Hooklets of sucker. c) Apical tegument with spiniform microtriches. 23. Rostellar hooks. 24. Sketch of male proglottides showing relative position of testes. 25. Early pregravid proglottis, dorsal view. 26. Gravid proglottides with developed capsules. Scale bars: 22 = 20 µm; 23 = 10 µm; 24, 26 = 100 µm; 25 = 50 µm.

Tables

Table 2. Main morphological characteristics of Raillietina hymenolepidoides sp. nov. and closely similar taxa. * New values from our observations of type material. Abbreviations: L = Length; W = Width; ø = Diameter.

	R. hymenolepidoides	R. palawanensis	R. quadritesticulata
Reference	Present study	Deardorff et al. (1976)	Moghe (1925)
Host	Chalcophaps indica	Chalcophaps indica	Streptopelia tranquebarica
Ditribution	Malaysia	Philippines	India
L [mm] × W	55 × 425	*> 60 × *790	62–137 × 924–1230
# proglottides	800 +	–	188–196
Scolex ø	100–137	300–320	165
Sucker ø	34–43	72–76	52–54 × 35–40
Rostellum ø (× L)	46–69	125–170 × 110–160	96
# hooks	150–160	108	180
L hooks	7–8	20–24	6
L neck [mm]	2.5	1.5–2.8	1
Dorsal canals	Absent	*Absent	Present (?)
Atrium L [mm] × W	7–13 × 9–21	6–15 × 7–26	–
Testes number	3	*(3)–4–5–(6)	4
Testes ø	35–50	45–57	68–75 × 75–77
Cirrus sac (L × W)	63–81 × 28–39	93–*120 × 28–*56	138 × 68
Copulatory vagina (L × W)	25–48 × 6–15	*39–52 × 10–17	108 × 32
Vitellarium (L × W)	26–35 × 17–26	25 × 30	–
# egg capsules	8–12	10–*17	40–50
Eggs per capsule	5–10	4–*7	6–8
# oncospheres	12–14	*16–18	18 × 16