Stillabothrium hyphantoseptum Herzog, Bergman et Reyda, 2016

Reyda, Florian B., Healy, Claire J., Haslach, Andrew R., Ruhnke, Timothy R., Aprill, Tara L., Bergman, Michael P., Daigler, Andrew L., Dedrick, Elsie A., Delgado, Illari, Forti, Kathryn S., Herzog, Kaylee S., Russell, Rebecca S. & Willsey, Danielle D., 2016, A new genus of rhinebothriidean cestodes from batoid elasmobranchs, with the description of five new species and two new combinations, Folia Parasitologica (038) 63 (38), pp. 1-28 : 14-16

Stillabothrium hyphantoseptum Herzog, Bergman et Reyda sp. n.

Figs. 1 , 8 , 9 , 16D

ZooBank number for species:

urn:lsid:zoobank.org:act:97362AA0-762D-4C87-B5ED-0A3664D69E98

Description (based on whole mounts of 29 complete mature worms, cross sections of 2 strobila and longitudinal sections of 2 scoleces and 2 scoleces prepared for SEM): Worms ( Fig. 8A ) euapolytic, acraspedote, 1.10–2.28 mm (1.64 ± 0.3; n = 29) long, greatest width 368–933 (601 ± 140; n = 29) at level of scolex; 5–9 (7.3 ± 1.1; n = 29) proglottids per worm. Cephalic peduncle lacking; small darkly staining germinative zone present.

Scolex ( Fig. 8B ) consisting of scolex proper bearing 4 stalked bothridia. Stalks 49–270 (119 ± 54; n = 22) long by 48–101 (73 ± 15; n = 27) wide, attached slightly posterior to middle of bothridia. Bothridia varying in shape with degree of contraction, from finely ovoid ( Fig. 8A ), broadly ovoid ( Fig. 8B ), to broadly deltoid ( Fig. 9A ), facially loculated, 247–390 (319 ± 35; n = 24) long by 213–360 (288 ± 37; n = 24) wide; bothridial margins with thin rim. Anterior region of bothridia ( Figs. 8A,B , 9B ) with 6–8 horizontally oriented loculi (i.e. loculi wider than long) with 6–8 complete transverse septa (7.2 ± 0.5; n = 26). Anteriormost loculus 30–51 (40 ± 6; n = 27) long by 54–90 (71 ± 10; n = 29) wide. Posterior region of bothridia with 8 (n = 21) nonmedial longitudinal septa dividing bothridia into 9 loculi longer than wide; majority of longitudinal septa overlapping posteriormost 3–6 (4.3 ± 0.9; n = 13) transverse septa of anterior region of bothridia, resulting in a grid-like pattern of septa and loculi in the centre of bothridium ( Fig. 8A,B ).

Loculi and septa of distal bothridial surfaces ( Fig. 9B ) bearing capilliform filitriches and coniform spinitriches. Proximal bothridial rim ( Fig. 9C,D ) bearing capilliform filitriches ( Fig. 9B ). Proximal bothridial surfaces away from rim bearing acicular filitriches throughout bothridium ( Fig. 9D,E,F ). Posterior margin of proximal bothridial surfaces bearing a patch of coniform spinitriches ( Fig. 9C,E ) near, but not extending to, bothridial rim. Bothridial stalks and strobila ( Fig. 9G ) bearing capilliform filitriches only.

Strobila with 2–5 (3.5 ± 0.9; n = 29) proglottids wider than long followed by 2–6 (3.9 ± 0.8; n = 29) proglottids longer than wide. Strobila widest at terminal proglottid; terminal proglottid 381–840 (601 ± 127; n = 29) long by 78–155 (12 ± 18; n = 29) wide; genital pore located 50–61% (55 ± 3.6; n = 29) of proglottid length from proglottid posterior margin. Immature proglottids 4–8 (6.0 ± 1.1; n = 29) in number. Mature proglottids 1–2 (1.3 ± 0.5; n = 29) in number, including 0–1 (0.6 ± 0.5; n = 29) vas deferens-mature proglottid.

Testes in mature proglottids 9–16 (13 ± 1.9; n = 28) in total number, 1 layer deep in section, arranged in 2 columns; columns extending from anterior margin of proglottid to anterior margin of cirrus sac, 23–57 (33 ± 7; n = 25) long by 27–49 (39 ± 7; n = 25) wide. Vas deferens coiled, entering anterior margin of cirrus sac, extending from level of ovarian isthmus to overlap posteriormost testes. Cirrus sac thin-walled, oval, extending medially past midline of proglottid; cirrus sac in terminal mature proglottid 45–69 (57 ± 6; n = 12) long by 38–60 (49 ± 7; n = 12) wide; cirrus sac in vas deferens-mature proglottids 52–79 (63 ± 8; n = 16) long by 45–63 (54 ± 5; n = 16) wide. Cirrus spinitriches present.

Vagina ( Figs. 8C , 16D ) thick-walled, weakly sinuous, somewhat overlapping medial portion of cirrus sac ( Fig. 8A ), extending along midline of proglottid from ootype region to anterior margin of cirrus sac, then laterally to open into genital atrium anterior to cirrus sac; vaginal sphincter absent. Seminal receptacle present. Ovary near posterior end of proglottid, H-shaped in frontal view, tetralobed in cross section. Ovarian lobes asymmetrical; poral ovarian lobe somewhat overlapping cirrus sac; poral and aporal ovarian lobes in terminal mature proglottids 125–201 (155 ± 28; n = 9) and 140–213 (165 ± 27; n = 9) long, respectively. Poral and aporal ovarian lobes in vas deferens-mature proglottids 175–290 (216 ± 27; n = 15) and 175–290 (228 ± 34; n = 15) long, respectively. Maximum width of ovary 68–114 (92 ± 12; n = 24). Ovarian isthmus at or anterior to midpoint of ovary; poral lobe of ovary stopping 30–80 (53 ± 14; n = 24) short of genital pore. Mehlis’ gland posterior to ovarian isthmus, 24–70 (40 ± 11; n = 20) long by 14–30 (21 ± 5; n = 18) wide. Vitellarium follicular, 1 dorsal and 1 ventral column on each side of proglottid; columns extending from anterior to posterior margin of proglottid, interrupted by terminal genitalia, and interrupted by ovary ( Fig. 8A,C ). Uterus ventral, sacciform, extending from posterior margin of proglottid to near anterior margin of proglottid.

T y p e a n d o n l y k n o w n h o s t: Pastinachus solocirostris Last, Manjaji et Yearsley, Roughnose stingray (Myliobatiformes: Dasyatidae ).

Ty p e l o c a l i t y: South China Sea off Mukah (02°53'52''N; 112°05'44''E), Sarawak, Malaysian Borneo (BO-267) .

A d d i t i o n a l l o c a l i t i e s: Java Sea off Singkawang (Pasar Bringin) (00°55'06''N; 108°58'58''E) , West Kalimantan, Indonesian Borneo (KA-148).

S i t e o f i n f e c t i o n: Spiral intestine.

Ty p e m a t e r i a l: Holotype MZUM (P) No. 2016.13 (H). Paratypes: IPCAS No. C-741; LRP Nos. 9003–9004; 9083– 9117 (including molecular vouchers, sec-tions, and SEM specimens); MZUM (P) No. 2016.14 (P)–2016.15 (P); SBC No. P-00072; USNM Nos. 1420471–1420477.

E t y m o l o g y: This species is named for the grid-like pattern of septa in the centre of the bothridium. The name is a combination of the Latin ‘hyphantos’, meaning woven, and the Latin ‘septum’.

Remarks. The most striking characteristic of S. hyphantoseptum sp. n. is the extensive grid-like appearance of the septa on the centre of the bothridia ( Fig. 8A,B ). This configuration results from the extensive overlap of transverse (anterior) septa and longitudinal (posterior) septa. This feature readily distinguishes S. hyphantoseptum from S. ashleyae and S. davidcynthiaorum , both of which lack overlapping septa. The only other described species of Stillabothrium with overlapping transverse and longitudinal septa is S. campbelli ( Fig. 6A,B ). Although the centre of bothridia of S. campbelli is grid-like, the grid-like area is less extensive than in S. hyphantoseptum (compare Figs. 6B and 8B ). In S. campbelli , the posteriormost 3–4 transverse septa are overlapped by its central 2 longitudinal septa, whereas in S. hyphantoseptum the posteriormost 3–6 transverse septa are overlapped by most of its eight longitudinal septa. The number of loculi that are wider than long in the anterior region of bothridia is also different between the two species (6–8 in S. hyphantoseptum vs 10–12 in S. campbelli ).

In terms of proglottid morphology, S. hyphantoseptum sp. n. can be distinguished from S. ashleyae , S. davidcynthiaorum and S. campbelli in its possession of a uterus that extends to the posterior margin of the proglottid ( Fig. 8C ), whereas in the latter three species the uterus only extends posteriorly to the ovarian isthmus ( Figs. 4C , 6C ; not illustrated for S. ashleyae , but observed).

Stillabothrium hyphantoseptum is the only species of Stillabothrium reported from a species of Pastinachus Rüppell. The host species, P. solocirostris (roughnose stingray) was described by Last et al. (2005) as part of the same survey work that made the current study possible.

Two specimens of S. hyphantoseptum were included in the phylogenetic analysis ( Fig. 1 , Table 1 ).

Figures

Fig. 1. Phylogram based on Bayesian analysis of 1084 bp region of D1–D3 28S rDNA. Numbers above branches indicate Bayesian posterior probabilities, numbers below indicate Bootstrap percentage values, based on 1000 replicates. Scale indicates expected num- ber of substitutions per site. Diagrammatic line drawings of fully opened bothridia of the seven described species mapped onto the clades representing those respective species. Host species information in Table 1.

Fig. 8. Line drawings of Stillabothrium hyphantoseptum sp. n. from Pastinachus solocirostris Last, Manjaji et Yearsley. A – whole worm (holotype; MZUM [P] 2016.13 [H]); B – scolex (LRP 9092); C – terminal proglottid (LRP 9088).

Fig. 9. Scanning electron micrographs of Stillabothrium hyphantoseptum sp. n. from Pastinachus solocirostris Last, Manjaji et Years- ley. A – scolex; letters indicate locations of other SEMs; B – distal bothridial surface at second loculus and transverse septum; C, D – proximal bothridial surface with rim; E – proximal bothridial surface near rim; F – proximal bothridial surface; G – strobila.

Fig. 16. Light micrographs of terminal genitalia of Stillabothrium species, each with genital pore oriented left. A – Stillabothrium ashleyae sp. n. from Dasyatis biasa (Last, White et Naylor); B – Stillabothrium davidcynthiaorum sp. n. from Himantura gerrardi (Gray); C – Stillabothrium campbelli sp. n. from Himantura cf. pastinacoides; D – Stillabothrium hyphantoseptum sp. n. from Pastinachus solocirostris Last, Manjaji et Yearsley; E – Stillabothrium jeanfortiae sp. n. from Himantura australis Last, White et Naylor; F – Stillabothrium cadenati comb. n. from Zanobatus schoenleinii (Müller et Henle).

Fig. 6. Line drawings of Stillabothrium campbelli sp. n. from Himantura cf. pastinacoides. A – whole worm (holotype; MZUM [P] 2016.11 [H]); B – scolex (LRP 9066); C – terminal proglottid (LRP 9067).

Fig. 4. Line drawings of Stillabothrium davidcynthiaorum sp. n. from Himantura heterura (Bleeker). A – whole worm (LRP 9046); B – scolex (holotype, MZUM [P] 2016.9 [H]); C – terminal proglottid (LRP 9046).