Revision of Gangesia (Cestoda: Proteocephalidea) in the Indomalayan region: morphology, molecules and surface ultrastructure

Abstract

Tapeworms of Gangesia Woodland, 1924 (Cestoda: Proteocephalidea) parasitic in freshwater fishes in the Indomalayan Region were critically reviewed. Evaluation of type specimens and newly collected materials from Bangladesh, Cambodia and India, as well as critical examination of extensive literature have shown that only the following four species, instead of 48 nominal species of Gangesia and Silurotaenia Nybelin, 1942 reported from this region (36 new synonymies proposed), are valid: Gangesia bengalensis (Southwell, 1913), type-species of the genus and most common parasite of Wallago attu (Siluridae), G. macrones Woodland, 1924 typical of Sperata seenghala (Bagridae), both species characterized by the possession of two circles of hooks on the rostellum-like organ and several rows of hooklets on the anterior margins of suckers; G. agraensis Verma, 1928 from W. attu (typical host), which has the scolex with only one circle of hooks and 1-3 incomplete rows of tiny hooklets on the suckers; and G. vachai (Gupta and Parmar, 1988) n. comb. from several catfishes, which possesses 4-6 circles of hooks and 5-11 rows of hooklets on the anterior half of suckers. Scolex morphology, including surface ultrastructure (microtriches), of all but one species (G. vachai) is described for the first time using scanning electron microscopy. A phylogenetic analysis based on the partial sequences encoding the large nuclear ribosomal subunit RNA gene has shown that three Indomalayan species, namely G. bengalensis, G. macrones and G. vachai, form a monophyletic group within Gangesia, whereas G. agraensis tends to form a clade with the Palaearctic species of the genus. A table with differential characters of all species from the Indomalayan Region is also provided together with a key to identification of genera of the subfamily Gangesiinae. The present study demonstrates that species of Silurotaenia do not occur in the Indomalayan region.

Figure 1. Gangesia bengalensis (Southwell, 1913) from Wallago attu, India. A.

Scolex, dorsoventral view (MHNG-PLAT 82308, field no. AA 133B). B. Rostellar hooks (IPCAS C-616, field no. AA 133). C. Detail of retractor muscles. D, E. Mature proglottides, ventral view (IPCAS C-616, field no. AA 133 and MHNG-PLAT 60721, field no. 147/08). F. Gravid proglottis, ventral view (IPCAS C-616, field no. AA 133). G, H. Cross sections at level of testicular field and ovary, respectively (IPCAS C-616, field no. AA 133); note that subtegumental layer is not fully illustrated. I. Egg drawn in distilled water. Abbreviations: ba – base of hook, bl – blade of hook, cs – cirrus-sac, doc – dorsal osmoregulatory canal, eh – embryonic hook, em – embryophore, ga – genital atrium, hl – hooklets, ho – hooks, ilm – internal longitudinal muscles, lub – lateral uterine branch, oe – outer envelope, on – oncosphere, ov – ovary, re – retractor muscles, ro – rostellum-like organ, sl – subtegumental layer, su – sucker, te – testes, us – uterine stem, uso – uterine slit-like opening, ut – uterus, va – vagina, vf – vitelline follicles, voc – ventral osmoregulatory canal, vs – vaginal sphincter.

Figure 2. Scanning electron photomicrographs of Gangesia bengalensis (Southwell 1913).

A. Scolex, dorsoventral view. B, C. Detail of rostellum-like organ; note two rows of rostellar hooks. D. Sucker with small hooklets on the outer rim. E. Detail of the outer rim of the sucker with hooklets. F. Detail of short, dense acicular filitriches on the rostellum-like organ. G. Detail of acicular filitriches and few capilliform filitriches on the sucker. H. Detail of capilliform filitriches and small gladiate spinitriches in between the suckers. I. Detail of gladiate spinitriches on the neck region. Scale bars: A –100 µm; B –10 µm; C, D –20 µm; E–I –1 µm.

Figure 3. Type specimens of Gangesia wallago Woodland, 1924 and G. sindensis Rehana and Bilqees, 1971. A.

Scolex of G. wallago, sub-apical view; note presence of two irregular rows of rostellar hooks ( = G. bengalensis) and hooklets (hl) on the sucker. B, C. Details of arrangement of hooks on a rostellum-like organ of G. wallago (B – G. agraensis; C – G. bengalensis); note two types of arrangement. D. Scolex of G. sindensis, dorsoventral view; note the presence of hooklets on the suckers. E. Details of arrangement of hooks on a rostellum-like organ of G. sindensis ( = G. bengalensis); note the presence of a double rows of hooks.

Figure 4. Gangesia agraensis Verma, 1928 from Wallago attu, India. A.

Scolex, dorsoventral view (IPCAS C-617, field no. IND 167). B. Rostellar hooks (MHNG-PLAT 82298, field no. IND 795B). C. Detail of retractor muscles. D. Terminal genitalia, dorsal view (IPCAS C-617, field no. IND 795). E. Mature proglottis, dorsal view (IPCAS C-617, field no. IND 167). F, G. Cross sections at level of testicular field and ovary, respectively (MHNG-PLAT 60725, field no. 117/08). H. Egg drawn in distilled water. I. Gravid proglottis, ventral view (IPCAS C-617, field no. IND 795). Abbreviations: doc – dorsal osmoregulatory canal, upo – uterine pore- like opening, voc – ventral osmoregulatory canal, vs – vaginal sphincter.

Figure 5. Scanning electron photomicrographs of the scolex of Gangesia agraensis Verma, 1928.

A. Scolex, dorsoventral view. B. Scolex, apical view. C. Sucker with small hooklets on the outer rim. D. Detail of rostellum-like organ, dorsoventral view; note one row of rostellar hooks. E. Detail of the outer rim of the sucker with hooklets. F. Detail of papilliform filitriches on the rostellum-like organ. G. Detail of papilliform filitriches on the sucker. H. Detail of acicular filitriches in between the suckers. I. Detail of capilliform filitriches and small gladiate spinitriches on the neck region. Scale bars: A –100 µm; B–D –20 µm; E, I –2 µm; F–H –1 µm.

Figure 6. Gangesia macrones Woodland, 1924 from Sperata seenghala, India. A.

Scolex, dorsoventral view (IPCAS C-618, field no. MS 4h). B. Rostellar hooks (IPCAS C-618, field no. MS 4h). C. Scolex of decomposed specimen fixed with cold formalin and detached hooks and hooklets (IPCAS C-618, field no. MH 26). D. Mature proglottis, ventral view (MHNG-PLAT 82302, field no. MS 6r). E. Terminal genitalia, ventral view (IPCAS C-618, MS 4h). F. Gravid proglottis, ventral view (IPCAS C-618, field no. MS 4h). G, H. Cross sections at level of testicular field and ovary, respectively (IPCAS C-618, field no. MS 4k). I. Eggs drawn in distilled water.

Figure 7. Scanning electron photomicrographs of the scolex of Gangesia macrones Woodland, 1924.

A, B. Scolex, dorsoventral view. C. Sucker with small hooklets on the outer rim. D. Detail of a rostellum-like organ; note two rows of rostellar hooks of different shape with capilliform filitriches. E. Detail of the outer rim of the sucker with hooklets and capilliform filitriches. F. Detail of capilliform filitriches on the rostellum-like organ. G. Detail of capilliform filitriches and gladiate spinitriches in between the suckers. H. Detail of capilliform filitriches on the sucker. I. Gladiate spinitriches on the neck region. Scale bars: A, B –30 µm; C –20 µm; D–F –2 µm; G–I –1 µm.

Figure 8. Gangesia vachai (Gupta and Parmar, 1988) n. comb. from Mystus sp., India and Wallago attu, Bangladesh. A.

Scolex of specimen from Wallago attu, dorsoventral view (MHNG-PLAT 82306, field no. BAN 186). B. Rostellar hooks; note different sizes (distributed in 4–6 rows) (MHNG-PLAT 82306, field no. BAN 186). C. Egg drawn in distilled water. D. Scolex of specimen from Mystus cf. tengara, dorsoventral view (IPCAS C-623, field no. IND 906a). E. Gravid proglottis, ventral view (MHNG-PLAT 82306, field no. BAN 186). F. Mature proglottis, ventral view (MHNG-PLAT 82306, field no. BAN 186). G. Cross sections at level of the ovary (IPCAS C-623, field no. IND 906a). H. Terminal genitalia, ventral view (MHNG-PLAT 82306, field no. BAN 186).

Figure 9. Outline of scoleces with retractor muscles of selected Gangesia and Silurotaenia taxa. A

–E. Outline of the scoleces with retractor muscles of Gangesia agraensis, G. bengalensis, G. macrones, G. vachai and Silurotaenia siluri, respectively. F, G. Frontal section of the scoleces of G. agraensis (IPCAS C-617, field no. AA 86a) and G. bengalensis (IPCAS C-616, field no. AA 133), respectively. H. Sagittal section of the scolex of G. macrones (MHNG-PLAT 82303, field no. MS 22b).

Figure 10. Phylogenetic analysis and lsrDNA total sequence differences of valid Gangesia taxa of the Indomalayan region along with all Palaearctic taxa available.

Note that individual OTUs might represent multiple Gangesia specimens sequenced bearing an identical lsrDNA sequence. Rooted phylogram. Total nucleotide differences between individual isolates are summarized in the boxed table.

Figure 11. Phylogenetic interrelationships of the subfamily Gangesiinae based on lsrDNA data.

Gangesia species with multiple specimens of unique lsrDNA sequence (G. agraensis, G. oligonchis, G. vachai) are depicted as single OTUs for clarity.