Anindobothrium danielae, García Facal & Franzese & Montes & Menoret, 2024

García Facal, Guillermina, Franzese, Sebastián, Montes, Martín Miguel & Menoret, Adriana, 2024, Molecular phylogeny, including a new species of Anindobothrium (Cestoda, Rhinebothriidea) from the Southern eagle ray Myliobatis goodei, finally solves the taxonomic enigma of Phyllobothrium myliobatidis, Zoosystematics and Evolution 100 (4), pp. 1401-1417 : 1401-1417

Anindobothrium danielae sp. nov.

Figs 2 , 3 , 4 , 5

Type material.

Holotype • an entire, mature worm, off Bahía San Blas , Buenos Aires Province, Argentina (40°42.92'S, 62°00.58'W), 23 m, 2 Apr 2013, A. Menoret leg., MACN-Pa No. 798 .

Paratypes • Three entire, mature worms, cross-section of 2 attached mature proglottids, same data as preceding, MACN-Pa No. 799 / 1–5 • Two entire, mature worms, same data as preceding, MLP-He No. 8136 • Six entire, mature worms, off Puerto Quequén , Buenos Aires Province (38°53.00'S, 58°27.00'W), 20 Jul 2001, V. A. Ivanov leg., MACN-Pa Nos. 795 / 1–2 and 800 / 1–4 • Two entire, mature worms, same data as preceding, MLP-He No. 8135 • One entire, mature worm, off Puerto Quequén , Buenos Aires Province, Argentina (38°53.00'S, 58°27.00'W), 22 Jan 2018, G. García Facal leg., MACN-Pa No. 796 • Three entire, mature worms, off Balneario San Cayetano , Buenos Aires Province, Argentina (38°54.01'S, 59°12.02'W), 37 m, 20 Feb 2018, G. García Facal & A. Menoret leg., MACN-Pa No. 797 / 1–3 • Cross-section of 1 scolex, off San Matías Gulf , Rio Negro Province, Argentina (41°11.00'S, 64°03.26'W), 73 m, 20 Mar 2011, A. Menoret & V. A. Ivanov leg., MACN-Pa No. 800 .

Description.

Based on 23 specimens in total: 18 entire, mature worms, cross-sections of 2 terminal mature proglottids, cross-sections of 1 scolex, and SEM of 2 worms. Worms euapolytic, 9.1–21.5 (14.2 ± 4.1, n = 17) mm long, 22–49 (32 ± 9, n = 17) acraspedote proglottids (Fig. 2 A ). Scolex 510–1,150 (775 ± 176, n = 17) long, 600–1,625 (1011 ± 309, n = 17) wide, composed of four stalked bothridia (Figs 2 B , 3 A ). Bothridia orbicular-shaped, 272–850 (561 ± 213, n = 7) long, 272–1,000 (729 ± 296, n = 7) wide, with 101–121 (115 ± 10, n = 5) marginal loculi and anterior apical sucker. Apical sucker 40–90 (64 ± 19, n = 6) long, 48–100 (66 ± 21, n = 6) wide (Figs 2 B, C , 3 A – C ). Transverse and longitudinal septa absent. Distal portion of marginal septa formed by marginal muscle bundles; proximal portion formed by radial muscles with proximal fibers ending adjacent to each other (Fig. 2 D ). Cephalic peduncle 410–1,400 (856 ± 292, n = 18) long, 100–300 (192 ± 63, n = 18) wide.

Apex of scolex proper covered with acicular filitriches (Fig. 3 D ). Proximal bothridial surface covered with acicular filitriches, cilia present in marginal loculi (Fig. 3 F ). Distal surface covered with capilliform filitriches and coniform spinitriches (Fig. 3 E ). Surface of bothridial stalks covered with acicular filitriches. Cephalic peduncle and anterior portion of strobila covered with capilliform filitriches (Fig. 3 G ).

Immature proglottid, initially wider than long, becoming longer than wide with maturity. Most terminal proglottids and some subterminal proglottids with sperm-filled vas deferens. Mature proglottids without sperm-filled vas deferens 1,080 –2,150 (1,491 ± 269, n = 18) long, 315–600 (423 ± 103, n = 18) wide, length to width ratio 2.3–5.3 (3.7 ± 0.9, n = 18): 1 (Figs 2 A , 4 A ). Terminal mature proglottids with sperm-filled vas deferens 1,525 –2,675 (2,013 ± 312, n = 15) long, 300–620 (427 ± 107, n = 15) wide, length to width ratio 3.1–6.8 (4.9 ± 1.0, n = 15): 1 (Figs 2 A , 4 B ), mature proglottids 2–7 (4 ± 1, n = 18) in number per worm (Fig. 2 A ). Gravid proglottids not observed.

Testes round to oval, 52–83 (68 ± 8, n = 17) long, 39–68 (55 ± 8, n = 17) wide, 76–115 (97 ± 11, n = 17) in number, 9–19 (13 ± 3, n = 17) preporal, 24–38 (32 ± 4, n = 17) postporal, 41–64 (51 ± 7, n = 17) aporal, arranged anteroposteriorly in 4 regular columns, 2 layers deep in cross-section; each column extending from anterior margin of proglottid reaching anterior margin of ovary (Figs 4 A, B , 5 A – C ). Cirrus sac pyriform in anterior third of proglottid, bent posteriorly, 103–200 (152 ± 32, n = 17) long, 43–135 (93 ± 26, n = 17) wide, containing coiled cirrus; cirrus covered with spinitriches (Figs 4 C , 5 C, F ). Vas deferens coiled, extending posteriorly at level of cirrus sac to near anterior margin of ovary, entering cirrus sac at anteromedial margin (Figs 4 A – C , 5 C, F ).

Vagina thick-walled, extending anteriorly from ootype, then running along midline of proglottid to anterior margin of cirrus sac, and laterally opening into genital atrium anterior to cirrus, vaginal sphincter present (Figs 4 C , 5 B, E ). Ovary H-shaped in frontal view, poral lobe 185–450 (314 ± 66, n = 17) long, aporal lobe 218–440 (310 ± 61, n = 17) long, 170–380 (266 ± 57, n = 17) wide at isthmus, tetra-lobed in cross-section (Figs 4 A, B , 5 D ). Mehlis’ gland posterior to ovarian isthmus, 65–115 (97 ± 16, n = 16) long, 70–120 (90 ± 17, n = 17) wide. Vitellarium follicular; vitelline follicles oval, 10–22 (15 ± 4, n = 16) long, 12–42 (27 ± 7, n = 16) wide, in 2 dorsal and 2 ventral columns on each lateral margin of proglottid, lateral to testes, extending from near anterior margin of proglottid to posterior margin of proglottid, partly interrupted by terminal genitalia and uninterrupted by ovary (Figs 4 A – C , 5 A – F ). Uterus saccate, medial, and ventral, extending from the level of the genital atrium to ovarian isthmus (Fig. 4 A – C ). Osmoregulatory ducts 4, 1 dorsal, and 1 ventral pair on each lateral margin of proglottid, dorsal pair larger than ventral pair (Figs 4 C , 5 A – C ).

Host.

Myliobatis goodei Garman, 1855 , Southern eagle ray ( Myliobatiformes : Myliobatidae ) (type host). Site of infection: spiral intestine. Prevalence of infection: 58 % (7 hosts infected out of 12 examined).

Sequence data.

GenBank accession numbers PQ 346665, PQ 346666; 2 hologenophores MACN-Pa No. 801 / 1-2.

Etymology.

This species is named after Daniela Barbieri, the first author’s dear friend, in appreciation for her continued support and enthusiasm for science.

Distribution.

Anindobothrium danielae sp. nov. occurs mainly along coastal waters off Buenos Aires Province, at depths of <100 m in the Warm Temperate SWA Marine Province.

Remarks.

Anindobothrium danielae sp. nov. can easily be distinguished from A. anacolum , A. carrioni , and A. inexpectatum by the morphology of the bothridia. The new species has orbicular-shaped bothridia without longitudinal and transverse septa, whereas the three congeners exhibit ellipsoid-shaped bothridia with longitudinal and transverse septa (Figs 2 C , 3 A , 6 ). Anindobothrium danielae sp. nov. is different from A. anacolum , A. carrioni , A. inexpectatum , and A. lisae by having more testes per proglottid (76–115 vs. 24–50, 21–31, 23–44, and 30–72, respectively) along with the presence of two rows of testes arranged dorsoventrally instead of one. Furthermore, A. danielae sp. nov. possesses similar orbicular-shaped bothridia as A. lisae but can be distinguished from the freshwater species by the number of marginal loculi (101–121 vs. 40–58) and ovary length (59–159 vs. 185–450).

Figures

Figure 2. Light micrographs of Anindobothrium danielae sp. nov. from Myliobatis goodei. A. Entire, mature worm (holotype MACN-Pa No. 798); B. Scolex (paratype MACN-Pa No. 799 / 2); C. Bothridium (paratype MACN-Pa No. 799 / 1); D. Longitudinal section of bothridium (paratype MACN-Pa No. 800). Abbreviations: l - loculus; mmb - marginal muscle bundles; ms - marginal septum; rm - radial muscle. Arrowhead indicates the apical sucker.

Figure 3. Scanning electron micrographs of Anindobothrium danielae sp. nov. from Myliobatis goodei. A. Scolex, small letters indicate locations of detail shown in B – G; B. Bothridial apical sucker; C. Bothridial marginal loculi; D. Detail of apex surface with acicular filitriches; E. Detail of distal bothridial surface with capilliform filitriches and coniform spinitriches; F. Detail of proximal bothridial surface of marginal loculi with acicular filitriches; arrowheads indicate cilia; G. Detail of cephalic peduncle surface with capilliform filitriches.

Figure 4. Line drawings of Anindobothrium danielae sp. nov. from Myliobatis goodei. A. Subterminal mature proglottid (holotype MACN-Pa No. 798); B. Terminal mature proglottid with sperm-filled vas deferens (holotype MACN-Pa No. 798); C. Detail of terminal genitalia of subterminal proglottid, ventral view, (paratype MACN-Pa No. 795 / 4).

Figure 5. Light micrographs of cross-sections of mature proglottids of Anindobothrium danielae sp. nov. from Myliobatis goodei. A. Testes anterior to the cirrus sac (paratype MACN-Pa No. 799 / 3); B. At the level of the vagina (paratype MACN-Pa No. 799 / 4); C. At the level of the cirrus sac; arrowhead indicates the entrance of the vas deferens to the cirrus sac (paratype MACN-Pa No. 799 / 3); D. At the level of the ovarian isthmus (paratype MACN-Pa No. 799 / 3); E. Detail of the vagina showing vaginal sphincter and pigmented cells (paratype MACN-Pa No. 799 / 3); F. Detail of the cirrus sac showing armed cirrus; arrowhead indicates the entrance of the vas deferens to the cirrus sac (paratype MACN-Pa No. 799 / 3). Abbreviations: ci - cirrus; cs - cirrus sac; do - dorsal osmoregulatory duct; lm - longitudinal muscle; ov - ovary; pc - pigmented cells; sp - sphincter; ts - testes; ut - uterus; vd - vas deferens; vf - vitelline follicle; vg - vagina; vo - ventral osmoregulatory duct.

Figure 6. Schematic representation of the bothridia shape in the genus Anindobothrium. A. Ellipsoid-shaped bothridia, species subset 1: A. anacolum, A. carrioni, and A. inexpectatum; B. Orbicular-shaped bothridia, species subset 2: A. danielae sp. nov., A. lisae, and A. myliobatidis comb. nov.