Gangesia mukutmanipurensis, Marick & Brabec & Choudhury & Scholz & Ash, 2023

Marick, Jit, Brabec, Jan, Choudhury, Anindo, Scholz, Tomáš & Ash, Anirban, 2023, The evolution of an ancient tapeworm lineage in its catfish hosts: vicariance, dispersal and diversification in Gangesiinae (Cestoda: Proteocephalidae), Zoological Journal of the Linnean Society 198, pp. 509-533 : 516-522

GANGESIA MUKUTMANIPURENSIS SP. NOV.

( FIGS 4–6 )

Z o o B a n k r e g i s t r a t i o n: u r n: l s i d: z o o b a n k. org:act: 142F33C8-72A5-4BDA-AEAE-B2F0DBAB5413

Description

Based on 16 specimens from Ompok bimaculatus from West Bengal, India, including three scoleces observed using SEM: strobila more than 158 mm long (N = 3), with acraspedote proglottids, up to 1.96 mm wide (N = 3), consisting of more than 143 proglottids (N = 3): 40– 94 immature (up to appearance of spermatozoa in vas deferens), four to five mature (up to appearance of eggs in uterus), 67–74 pregravid (up to appearance of hooks in oncospheres) and gravid. Proglottids variable in shape, usually slightly wider than long in mature and pregravid and longer than wide in gravid towards terminal end; mature proglottids 575–1038 (733) long by 725–1413 (990) wide, L/W = 0.43–1.59 (0.79) (N = 18) .

Inner longitudinal musculature well-developed, anastomosed, forming isolated bundles of muscle fibres ( Fig. 4C, D ). Subtegumental muscles well-developed ( Fig. 4C, D ). Osmoregulatory canals running alongside vitelline follicles. Ventral osmoregulatory canals thin-walled, width representing 4–7% of width of mature proglottids, overlapping lateral-most testes, form anastomoses in some proglottids. Dorsal osmoregulatory canal narrow, thick-walled, prominent in immature proglottids but gradually disintegrating with maturation of proglottids, not observable in gravid proglottids, canal may reach lateral-most testes ( Figs 4A, B , 5E ).

Scolex wider than neck, 134–203 (157) long by 144–203 wide (169) (N = 7). Rostellum-like organ 34–61 (51) long and 53–89 (71) wide, devoid of hooks. Suckers four, uniloculate, devoid of hooklets on rims ( Figs 5A–C , 6A, B ), 59–89 (76) in diameter (N = 17); R/S = 0.75–1.14 (0.93), R/X = 0.35–0.50 (0.41).

Prominent retractor muscle bundles surrounding rostellum-like organ, joining at level of suckers, forming a wide band of muscles (retractors) in neck region ( Fig. 5B–D ).

Rostellum-like organ covered with capilliform filitriches ( Fig. 6C–G ), apical part additionally armed with several rows of large, coniform spinitriches ( Fig. 6A–C, H ). Suckers also covered with capilliform filitriches, rim of suckers with coniform spinitriches that are smaller than those on rostellum ( Fig. 6D–F ). Surface of scolex between suckers bearing interspersed gladiate spinitriches ( Fig. 6I ).

Proliferative zone 4.7–7.2 mm long and 333–416 wide (N = 2). Neck region covered with gladiate spinitriches.

Testes medullary, in single field, spherical to oval, 31–81 (50) in diameter (N = 115), numbering 82–144 (109) (N = 28), mostly forming single layer ( Figs 4A, B , 5E ), occupying 65–80% of length of proglottids. Cirrus-sac elongate, thick-walled, 163–269 (199) long by 63–88 (74) wide [N = 17; L/W = 2.0–3.7 (2.7)]; C/P = 17–26% (20%), i.e. 1/6–1/4 of width of proglottids. Genital pore irregularly alternating, pre-equatorial, situated at 23–40% (32%) (N = 13) of length of proglottids from anterior margin ( Figs 4A, B , 5E ).

Ovary medullary, 175–338 (228) long, 400–913 (640) wide (N = 18), occupying 26–38% (31%) of length of proglottid, bilobed, each lobe spherical to rectangular ( Figs 3A, B , 4E ); O/P = 55–71% (65%) (N = 18). Mehlis’ gland 81–113 (96) in diameter (N = 8), representing 8–11% of width of proglottid. Vagina thick-walled, posterior (58%) or anterior (42%, N = 100) to cirrus-sac, with higher concentration of chromophilic cells in its distal (terminal) part; ring-like vaginal sphincter present near genital atrium ( Figs 4A, B , 5E, F ).

Vitelline follicles oval, medullary, some follicles paramuscular (between muscle fibres of inner longitudinal musculature to cortex) ( Fig. 4C, D ), present in two longitudinal bands on lateral margin of proglottid, occupying 77–91% (86%) of length of proglottid on poral side, 85–96% (92%) on aporal side in mature proglottids (N = 17); bands interrupted at level of terminal genitalia on ventral side, with few follicles on dorsal side in more than half of mature and pregravid proglottids bands mostly interrupted (92%), both dorsally and ventrally in gravid proglottids ( Figs 4A, B , 5E, F ). Uterus medullary, with type 1 development (sensu de Chambrier et al., 2004). In pregravid proglottids, lateral diverticula thin-walled, 17–23 (20) in number on each side (N = 18), occupying up to 58% of proglottid width, may partly overlap ovary ( Fig. 4A, B ). Uterus with uterine pores; uterine pores four to seven in number (N = 18), slit-like ( Figs 4A , 5E ).

Eggs with hyaline, spherical outer envelope, 41–61 (50) in diameter (measured in eggs liberated from uterus in distilled water; N = 15); oncosphere spherical, 13–19 (16) in diameter, with three pairs of embryonic hooks, eight to 8–11 (9) long (N = 30), diameter with embryophore 20–30 (26); embryophore 2–5 (3) thick, consisting of two layers, outer layer thinner than nucleated inner envelope ( Fig. 5G ).

Taxonomic summary

Ty p e h o s t: O m p o k b i m a c u l a t u s (B l o c h, 1 7 9 4) ( Siluriformes : Siluridae ).

Site of infection: Intestine (anterior part).

Type locality: Mukutmanipur Dam Lake , Bankura , West Bengal, India (22°57’48"N, 86°47’18"E).

PreƲalence and intensity of infection: Prevalence 9.5% (20 of 211 Ompok bimaculatus examined); mean intensity 1.8 (one to four worms/host) (see Table 2 ).

Specimens deposited: Holotype and hologenophore ZSI/W11082/1/1–ZSI/W11083/1/2 . Paratypes: HWML-216818 ; IPCAS C-913/1 ; MHNG-PLAT-0067053 ; ZSI/W11084/1 , ZSI/W11085/1 , ZSI/W11086/1 , ZSI/W11087/1 , ZSI/W11088/1 , ZSI/W11089/1.

Genetic data: lsr DNA gene sequence (partial) (GenBank accession numbers) ON181446 , ON181456 , ON181457 and COI gene sequence (partial) (GenBank accession numbers) ON176195 . Hologenophores: MHNG-PLAT- 0067053; ZSI / W 11087 /1, ZSI / W11082/1/1–ZSI/W11083/1/2.

Etymology: The species name is derived from the Mukutmanipur Dam Lake, the type locality of this parasite.

Remarks: The new species is a member of Gangesia because it possesses characteristics that include: (1) presence of prominent retractor muscles that form a wide band; (2) rostellum-like organ longer than, or as long, as the size of suckers; (3) ventral osmoregulatory canals median (internal) to vitelline follicles; (4) testes in single field; (5) vagina posterior or anterior to the cirrus-sac; (6) lateral band of vitelline follicles occupying almost the total length of the proglottid; and (7) type 1 uterine development (sensu de Chambrier et al., 2004) (see ‘Generic composition and interrelationship in the Gangesiinae’ in the Discussion for details). The new species differs from all eight congeners by the absence of hooks on the rostellum-like organ and hooklets on the anterior rim of suckers, previously considered to be the most typical feature of the genus. Instead of hooks and hooklets, several rows of coniform spinitriches are present on the rostellum-like organ and the anterior rim of the suckers. Along with this unique scolex morphology, the new species is also typified by a narrow rostellum-like organ (less than 90 µm wide) and indistinguishable dorsal osmoregulatory canals in pregravid and gravid proglottids.

Figures

Figure 3. Simplified relationships among the genera of the subfamilies Gangesiinae and Acanthotaeniinae after collapsing nodes with SH-aLRT ≤ 80% and BS ≤ 70–80% on the phylogenetic tree in Figure 2. This simplified tree, having essentially similar topology once the poorly supported nodes on the lsrDNA tree are collapsed, provides the basis for discussions of historical biogeography.

Figure 4. Line drawings of Gangesia mukutmanipurensis sp. nov. from Ompok bimaculatus (specimen accession number in parentheses). A, gravid proglottid, ventral view (ZSI/W11083/1/2). B, gravid proglottid, dorsal view (ZSI/W11083/1/2). C, D, cross-sections at level of testicular field and ovary, respectively (ZSI/W11088/1 and ZSI/W11089/1). Abbreviations: doc, dorsal osmoregulatory canal; ilm, internal longitudinal muscles; lud, lateral uterine diverticula; Mg, Mehlis’ gland; ov, ovary; sl, subtegumental layer; te, testes; ut, uterus; vf, vitelline follicles; voc, ventral osmoregulatory canal.

Figure 5. Line drawings of Gangesia mukutmanipurensis sp. nov. from Ompok bimaculatus (specimen accession number in parentheses). A, scolex, subapical view (ZSI/W11086/1). B, C, scolex, dorsoventral view (ZSI/W11085/1 and ZSI/W11082/1/1). D, frontal section of the scolex (ZSI/W11087/1). E, mature proglottid, ventral view (ZSI/W11084/1). F, terminal genitalia (ZSI/W11083/1/2). G, egg drawn in distilled water. Abbreviations: cc, chromophil cell; cs, cirrus-sac; doc, dorsal osmoregulatory canal; eh, embryonic hook; em, embryophore; ga, genital atrium; mi, microtriches; oc, osmoregulatory canal; oe, outer envelope; on, oncosphere; ov, ovary; re, retractor muscles; ro, rostellum-like organ; su, sucker; te, testes; up, uterine pore; va, vagina; vf, vitelline follicles; voc, ventral osmoregulatory canal; vs, vaginal sphincter.

Figure 6. Scanning electron micrographs of Gangesia mukutmanipurensis sp. nov. from Ompok bimaculatus. A, scolex, subapical view. B, scolex, dorsoventral view. C, detail of rostellum-like organ. D, sucker with coniform spinitriches on the outer rim. E, F, detail of outer rim of the sucker with coniform spinitriches. G, detail of capilliform filitriches on the rostellumlike organ. H, detail of coniform spinitriches on the rostellum-like organ. I, detail of gladiate spinitriches on the neck region.

Tables

Table 2. Prevalence and intensity of infection in Bankura, West Bengal, India

Locality	Month/ Year	No. of fish examined	No. of fish infected	Prevalence	Intensity (mean)
Mukutmanipur Dam Lake, Bankura	March/2009	12	1	8%	1 (1)
	Jan/2019	37	2	5%	2–4 (3)
	Feb/2019	56	9	16%	1–4 (1.44)
	March/2019	37	3	8%	2–4 (3)
	April/2019	15	0	0%	0 (0)
	Oct/2019	34	0	0%	0 (0)
	Jan/2020	20	5	25%	1–2 (1.4)