Acanthobothrium garciaprietoi, Rodríguez-Ibarra & Violante-González & Monks, 2023

Rodriguez-Ibarra, Erick, Violante-Gonzalez, Juan & Monks, Scott, 2023, Two new species of Acanthobothrium Blanchard, 1848 (Cestoda, Onchoproteocephalidea) from Urobatis jamaicensis (Cuvier, 1816) (Elasmobranchii, Batoidea, Myliobatiformes) of the Mexican Caribbean, ZooKeys 1169, pp. 175-201 : 175

Acanthobothrium garciaprietoi sp. nov.

Figs 3 , 4 , 5

Type material.

Holotype (CNHE-11881), 1 paratype (CNHE-11882), 4 paratypes (CHE-P00146), 1 paratype (HWML-216977).

Type host.

Urobatis jamaicensis (Cuvier, 1816) ( Elasmobranchii: Myliobatiformes : Urotrygonidae ).

Type locality.

Isla Contoy, Playa Ixmapoit (21°31'44.45"N, 86°48'11.53"W) Quintana Roo, Mexico.

Site of infection.

Spiral valve.

Prevalence of infection.

14.28%

Etymology.

The species is named in honor of M. C. Luis García-Prieto (Universidad Nacional Autónoma de México, Instituto de Biología, México) for his friendship and for his contributions to the knowledge of helminths.

Diagnosis.

Acanthobothrium garciaprietoi sp. nov. is a Category 1 species. Body small; relatively robust bothridia; large apical suckers; 7-9 proglottids; long hooks; 18-26 testes per proglottid; cirrus sac and the vagina share a common opening within the genital atrium; arms of ovary symmetrical.

Description.

(Based on 4 complete worms and 9 partial worms mounted on slides.) Entire worms 1.3 mm-2.1 mm (1.8 mm ± 0.4 mm, 4, 4) long; greatest width at scolex, euapolytic; 7-9 (8 ± 1, 4, 4) proglottids per worm (Figs 3 , 4 ). Scolex consisting of scolex proper and cephalic peduncle; scolex proper with four bothridia, 225-320 (278 ± 32; 13, 6) long by 275-323 (305 ± 19; 13, 6) wide; scolex covered with microtriches (gladiate spinitriches and papilliform filitriches, see Chervy 2009) (Fig. 5 ). Maximum width of scolex at level of middle loculus (Figs 3 - 5 ). Bothridia free posteriorly, 245-313 (274 ± 21; 13, 22) long by 135-160 (147 ± 8, 13, 22) wide; each with three loculi separated by two transverse septa, and specialized anterior region in form of muscular pad. Muscular pad 76-83 (79 ± 5, 12, 22) long by 95-110 (101 ± 5, 12, 22) wide, with apical sucker 28-35 (32 ± 3, 12) long by 28-35 (32 ± 2, 12, 22) wide, each with one pair of bipronged hooks at posterior margin (Figs 3 - 5 ). Anterior loculus of bothridia 133-168 (154 ± 10, 12, 22) long, middle loculus 50-83 (66 ± 11, 12, 22) long, posterior loculus 50-83 (65 ± 11, 12, 22) long; loculus length ratio 1:0.4:0.4 (anterior:middle:posterior). Velum present between medial margins of bothridia at posterior margin of middle loculus (Figs 3 - 5 ).

Hooks bipronged, hollow, with tubercle on the proximal surface of the axial prong; internal channels of axial and abaxial prongs continuous, smooth, the base and anterior part of each hook embedded in muscular pad; axial prongs much longer than abaxial prongs (Figs 3 - 5 ). Bases (handles) of medial and lateral hooks articulated with each other; lateral and medial hooks approximately equal in size (Figs 3 - 5 ). Lateral hook measurements: A 28-38 (33 ± 2; 14, 25), B 90-105 (96 ± 3; 13, 25), C 78-83 (80 ± 2; 13, 24), D 115-135 (122 ± 6; 13, 24). Medial hook measurements: A’ 25-35 (31 ± 3; 13, 25), B’ 93-110 (102 ± 5; 13, 26), C’ 75-88 (81 ± 3; 13, 26), D’ 115-135 (128 ± 5; 13, 26).

Cephalic peduncle 175-288 (232 ± 35, 13, 7) long by 58-90 (74 ± 11, 13, 7) wide, covered with coniform spinitriches (see Chervy 2009). Proglottids acraspedote. Immature proglottids 133-238 (181 ± 36, 7, 10) long by 93-188 (149 ± 32, n = 10) wide; mature proglottids 260-618 (401 ± 108, 9, 12) long by 133-233 (203 ± 27, 9, 13) wide; terminal mature proglottids 365-550 (480 ± 100, 3, 3) long by 103-205 (169 ± 58, 3, 3) wide (Figs 3 - 5 ). Gravid proglottids not observed. Genital pores marginal, irregularly alternating, 26-46% (34 ± 6%, 9, 13) of proglottid length from anterior end in terminal mature proglottids 34-40% (37 ± 3%, 3, 3). Testes oval in dorsoventral view, arranged irregularly anterior to ovarian lobes, two layers deep; testes 30-55 (39 ± 6, 9, 27) long by 50-75 (59 ± 6, 9, 27) wide; testes 18-26 (22 ± 2, 9, 12) in total number, 10-14 (11 ± 1, n = 12) aporal, 3-6 (5 ± 1, 9, 12) preporal, 5-7 (6 ± 1, 9, 12) postporal; no testes located posterior to ovarian isthmus (Figs 3 , 4 ).

Cirrus sac pyriform, 98-143 (125 ± 12, 9, 13) long, 30-88 (50 ± 15, 9, 13) wide in mature proglottids. Cirrus expanded at base, armed with spinitriches. Vagina thick walled, walls covered with gland cells, extending along medial line of proglottid from oötype, reaching to anterior margin of cirrus sac to common genital atrium; vaginal sphincter absent; seminal receptacle not seen. Vagina canal descends on the aporal side of proglottid relatively to the midline of proglottid, often with loops. Ovary with symmetrical lobes; poral lobe 133-375 (241 ± 79, 8, 3) long in mature proglottids, reaching to cirrus sac; aporal lobe 130-375 (240 ± 78, 8, 3) long, extending to the anterior margin of the cirrus sac. Ovary inverted A-shaped in dorsoventral view, lobulated, ovarian isthmus posterior to mid-point of ovary. Mehlis’ gland posterior to ovarian isthmus (Figs 3 , 4 ).

Vitellarium follicular, consisting of two lateral bands; each band consists of two columns of relatively large, elongate to oval follicles, extending from near anterior margin of proglottid to near posterior margin of proglottid, interrupted by vagina and cirrus sac; follicles 345-425 (391 ± 23, 3, 9) long, 14-22 (17 ± 3, 3, 9) wide. Uterus thin-walled, sacciform, extends from near anterior part of proglottid to near oӧtype. Excretory ducts lateral. Eggs not seen.

Remarks.

This is the third species of Acanthobothrium described from U. jamaicensis . Acanthobothrium garciaprietoi sp. nov. is a category 1 species (sensu Ghoshroy and Caira 2001; Zaragoza-Tapia et al. 2020a): specimens of this species have a total length ≤ 15 mm (worms = 1.3-2.1 mm long); the number of proglottids is ≤ 50 proglottids (the new species has 7-9 proglottids); the number of testes per proglottids is ≤ 80 (the new species has 18-26 testes) and the arms of the ovary are symmetric.

Currently, in Category 1, there are 57 species ( Ghoshroy and Caira 2001; Fyler and Caira 2006; Franzese and Ivanov 2020; Zaragoza-Tapia et al. 2020a) but only 12 species inhabit the eastern coast of the Americas: A. fogeli , A. lentiginosum , A. lineatum , A. schalli , A. ulmeri , and A. westi have been reported for the northern Gulf of Mexico; A. marplatensis , A. stefaniae , A. carolinae and A. domingae have been reported from the South Atlantic, and A. cartagenensis , and A. himanturi from the Caribbean Sea.

However, A. garciaprietoi sp. nov. should be compared with the species assigned to Category 2 that inhabit the same geographical region because the species in Categories 1 and 2 are similar; the two categories differ only in relation to the symmetry of the ovarian arms. Of the 55 species that are included in Category 2, only two have been reported from the same host and/or to inhabit the same general region: A. tasajerasi and A. urotrygoni , both from the Caribbean Sea (Table 1 ).

Of the species of Acanthobothrium in category 1, all except A. stefaniae , have acraspedote strobili; some are euapolytic or apolytic, and some are hyperapolytic. Members of Acanthobothrium known from the Gulf of Mexico are A. fogeli , A. lentiginosum , A. lineatum , A. schalli , A. ulmeri , and A. westi . Acanthobothrium garciaprietoi sp. nov. differ from A. fogeli , A. lineatum , and A. schalli by being shorter, with fewer proglottids, and less testes, except A. lentiginosum , A. ulmeri and A. westi , which overlap in total length, number of proglottids, number of testes and in the diameter of the accessory sucker. Acanthobothrium lentiginosum is similar to the new species. However, it has a scolex that, on the average, is longer (288-474 vs. 225-320), and somewhat longer bothridia (272-474 vs. 245-313) with longer loculi; the hooks have a longer abaxial prong (80-110 vs. 78-83), the cephalic peduncle is longer (288-456 vs. 175-288) and the genital pore is differently positioned (59-69 vs. 26-46, respectively). Acanthobothrium ulmeri differs from the new species by having a larger scolex (357-464 vs. 225-320), longer bothridia (281-432 vs. 245-313) and larger loculi; the hooks are shorter, with the axial prong (61-78 vs. 90-105) long and the abaxial prong (59-72 vs. 78-83) long; prongs that are both shorter in total length (77-103 vs. 115-135), and the cephalic peduncle is shorter (48-176 vs. 175-288). Acanthobothrium westi differs from the new species in having the scolex and smaller loculi (215-277 vs. 225-320, respectively), hooks with shored handles (25-28 vs. 28-38), axial prongs (42-53 vs. 90-105), and the abaxial prongs (38-48 vs. 78-83); the cephalic peduncle is longer (216-480 vs. 175-288), the cirrus sac is shorter (72-84 vs. 98-143), and range in the number of testes is less (20-24 vs. 18-26).

Of the species of Acanthobothrium reported from the South Atlantic, A. marplatensis , is much larger (4.79 mm-8.44 mm vs. 1.3 mm-2.1 mm for the new species), it has a greater number of proglottids (18-30 vs. 7-9, respectively), more testes per proglottid (24-39 vs. 18-26). The hooks of A. marplatensis are shorter, the cirrus sac rises towards the anterior end of the proglottid and the cirrus sac of the new species extends horizontally in mature proglottids (Fig. 3C ) or slightly posterior in some terminal proglottids. Acanthobothrium stefaniae has craspedote proglottids and is hyperapolytic; it has a smaller scolex (285-400 vs. 225-320), somewhat longer bothridia (247-355 vs. 245-313) and longer anterior loculi; the handles of the hooks are relatively shorter (25-32 vs. 28-38), the abaxial prongs are shorter (32-52 vs. 78-83), the axial prong is longer (102-112 vs. 90-105). In A. stefaniae , the genital pore opens at approximately mid-proglottid and, in A. garciaprietoi sp. nov., it opens at the anterior third of the proglottid.

Acanthobothrium cartagenensis and A. himanturi have been reported from the Caribbean Sea. Acanthobothrium cartagenensis differs from and A. garciaprietoi sp. nov. by having a greater number of proglottids (13 vs. 7-9, respectively); its scolex is square (300-300), while that of A. garciaprietoi sp. nov. is wider than long (225-320 long 275-323 wide); the loculi of A. cartagenensis are shorter (1:0.3:0.3 vs. 1:0.4:0.4). The apical pads of A. cartagenensis are 67 in diameter, and they are relatively elliptical with no invaginations in the hook region; in contrast, those of A. garciaprietoi sp. nov. are larger (76-83 long by 95-110 wide), with an invagination in the region between the hooks. The cephalic peduncle of A. caragenensis is shorter than that of A. garciaprietoi sp. nov. (180 long by 120 wide vs. 175-288 long by 58-90 wide). The testes of A. cartagenensis are smaller in diameter (30-45 vs. 50-75 long by 30-55 wide of A. garciaprietoi sp. nov.), but the cirrus sac of A. garciaprietoi sp. nov. is larger. The lobes of the ovary of A. cartagenensis are longer than those of A. garciaprietoi sp. nov. (210-390 long by 60-112 wide vs. 133-375 long).

Acanthobothrium himanturi differs from the new species by being longer (3.84-9.3 mm vs. 1.3-2.1 mm, respectively), slightly large scolex (240-350 vs. 225-320), longer bothridia (297-432 vs. 245-313) and longer cephalic peduncle (300-1,000 vs. 175-288). The handles of the hooks of A. himanturi are 43-61 long, the abaxial prong is 73-99 long, and the axial prong is 86-116 long, all being longer (28-38, 78-83, 90-105, respectively) than those of A. garciaprietoi sp. nov. It has a greater number of testes (38-57 vs. 18-26) and the ovarian lobes are longer and narrower (480-600 vs. 133-375) than those of A. garciaprietoi sp. nov.

Compared to the other two species in Categories 1 and 2, A. garciaprietoi sp. nov. differ from A. carolinae by the shorter body (1.3 mm-2.1 mm vs. 1.81mm-3.93, respectively), smaller number of proglottids (7-9 vs. 8-17), and the larger hooks. The new species A. garciaprietoi sp. nov., differs from A. domingae by the body size (1.3 mm -2.1 mm vs. 3.5 mm -5.4 mm, respectively), the number of proglottids (7-9 vs. 14-18, respectively), and the smaller hooks (115-135 vs. 168-238, respectively).

Figures

Figure 3. Acanthobothrium garciaprietoi sp. nov. holotype (CNHE- 11881). A scolex B pair of hooks C mature proglottid D terminal mature proglottid. Scale bars: 70 μm (B); 200 μm (A, C); 400 μm (D).

Figure 4. Acanthobothrium garciaprietoi sp. nov. A-D holotype (CNHE- 11881) E paratype (CNHE- 11882) A scolex B pair of hooks C mature proglottid D terminal mature proglottid E complete tapeworm, 400 μm. Scale bars: 100 μm.

Figure 5. Acanthobothrium garciaprietoi sp. nov. SEM images. Paratype (not deposited) A scolex B bothridial muscular pad with pair of hooks C central area of scolex proper between the bothridia D gladiate spinitriches located on the proximal bothridial surface, see image C E papilliform filitriches located on the scolex proper, behind the bothridia, see image C F coniforme spinitriches located on the cephalic peduncle. Scale bars: 5 μm (D-F); 30 μm (C); 100 μm (A, B).