Otobothrium crenacolle Linton, 1890

Beveridge, Ian & Justine, Jean-Lou, 2007, Redescriptions of four species of Otobothrium Linton, 1890 (Cestoda: Trypanorhyncha), including new records from Australia, New Caledonia and Malaysia, with the description of O. parvum n. sp., Zootaxa 1587, pp. 1-25 : 2-7

Otobothrium crenacolle Linton, 1890

( Figs 1–8 )

Types: neotype, USNPC 7695.

Type host: Sphyrna zygaena (Linnaeus, 1758) .

Type locality: Woods Hole, Massachusetts, USA, 7.viii.1914, coll. E. Linton.

Site in host: spiral valve.

Material examined: From Sphyrna zygaena (Linnaeus, 1758) : neotype; 6 specimens ("hammer head shark"), Woods Hole, Massachusetts, USA ( NHMG Inve 37282); from Carcharhinus melanopterus (Quoy & Gaimard, 1824) : 2 specimens, Darwin Harbour, NT, Australia ( SAM 29100); from Carcharhinus limbatus (Valenciennes, 1839) : 1 specimen, Darwin Harbour, NT, Australia ( SAM 29079); 60 specimens, Fog Bay, NT, Australia ( SAM 29099); 3 specimens, Sampan Mouth, Mary River, NT, Australia ( SAM 29098); from Lamiopsis temmincki (Müller & Henle, 1839) : 12 specimens, off Mukah, Sarawak, Malaysia ( USNPC 99270, MZUM 572-3).

Re-description: Neotype from Sphyrna zygaena , Wood's Hole, USA. Length 6.9 mm, with c.20 segments. Scolex craspedote, length 420, maximum width in region of pars bulbosa 210; pars bothrialis 190, bothrial pits 18–22 (20, n=2) in diameter; pars vaginalis 340; bulbs 75–80 (78, n=4) long, 35–50 (43, n=4) wide; terminal segment 1500 long, 240 wide; genital pore to posterior end 620; genitalia not fully developed; total number of testes 115, with 37 post-ovarian, 3 between ovary and genital atrium, 75 in remainder of segment; genitalia not fully developed; terminal genital ducts not visible.

Based on 5 specimens from Sphyrna zygaena, Woods Hole , USA ( NHMG). Small cestodes, 13.2–15.9 (14.1, n=5) mm long, with 24–27 (26, n=5) segments. Scolex craspedote, 385–435 (400, n=5) long, maximum width in region of pars bulbosa 154–177 (169, n=5). Two broad bothria, pars bothrialis 169–250 (216, n=5) long; paired bothrial pits, 19–28 (23, n=10) in diameter at opening, situated on posterior margin of bothrium. Pars vaginalis longer than pars bothrialis, 266–335 (293, n=5) long; tentacular sheaths sinuous. Bulbs almost spheroidal, 69–92 (81, n=5) long, 54–65 (58, n=5) wide; prebulbar organ absent; retractor muscle originates in anterior part of bulb; pars post-bulbosa absent.

Tentacles with very slight basal swelling; diameter in basal region 13–20 (16, n=5), in distal region 10–15 (13, n=5). Armature heteroacanthous, atypical, heteromorphous; hooks hollow. Hook files begin on internal surface of tentacle, terminate on external surface; 6 hooks per row; space present between hook files 1 and 1’ on internal surface of tentacle. Distinctive basal armature absent. Hooks 1(1’) large, uncinate, with broad base, 8.5–10 (9.4, n=5) long, base 7.0–10.0 (8.6, n=5) long; hooks 2(2’), erect, with broad blade and relatively long base, 7.7–10.0 (9.1, n=5) long, base 5.4–7.7 (6.5, n=5) long; hooks 3(3’) more slender, falcate, with shorter base, 6.9–9.2 (7.9, n=5) long, base 3.9–5.4 (4.8, n=5) long; hooks 4(4’) shorter, falcate, with smaller bases, 4.6–5.4 (5.1, n=5) long, base 3.5 (3.5, n=2) long; hooks 5(5’) short, spiniform, 3.1–3.9 (3.5, n=5) long; hooks 6(6’) short, spiniform, 1.5–2.3 (2.0, n=5) long. In metabasal region, single hook between each principal row; intercalary hooks spiniform, 1.0–2.3 (1.4, n=5) long; 2– 3 intercalary hooks per row; in basal region; in basal region, on external surface, initial 5 rows of tiny, spiniform hooks 1.5–3.1 (1.7, n=5) long; subsequent 4–5 rows consist of erect hooks sharply recurved at tips, 3.1–3.9 (3.5, n=5) long, base 0.4–1.2 (0.8, n=5) long.

Mature segments elongate, acraspedote, 2.25–3.02 (2.66, n=5) mm long, maximum width 250–349 (277, n=5); segment length: width ratio 7.9–12.3 (9.7, n=5); genital pores alternate irregularly, 540–1090 (830, n=5) from posterior end of segment. Densely staining areas anterior and posterior to genital atrium. Hermaphroditic sac thin-walled, 54–81 (67, n=5) long, 44–56 (50, n=5) wide. Cirrus joins vagina in distal part of hermaphroditic sac; cirrus corrugated, muscular, unarmed, leads to small, crescentic internal seminal vesicle at proximal pole of hermaphroditic sac; external seminal vesicle absent, but initial coils of vas deferens with distinctive cellular wall. Vas deferens coils posteriorly to ovarian isthmus. Testes intervascular, arranged often but not always in 2 columns, in single layer throughout medulla, not reaching anterior part of segment; testes 99–178 (128, n=10) long, 57–121 (85, n=10) wide; total number of testes per segment 118–139 (128, n=5), with 31– 41 (36, n=5) post-ovarian, 1–3 (2, n=5) post-vaginal, and 81–106 (90, n=5) prevaginal/aporal. Vagina penetrates proximal pole of hermaphroditic duct, then runs posteriorly to ovarian isthmus; seminal receptacle absent. Ovary bilobed in dorso-ventral view, tetra-lobed in transverse section, lobes 48–118 (70, n=5) long, 39–72 (43, n=5) wide; Mehlis’ gland posterior to ovarian isthmus, 30-48 (37, n=5) in diameter. Vitelline follicles circum-medullary, 20–30 (27, n=5) in diameter. Uterine duct coils anteriorly from Mehlis’ gland to level of hermaphroditic sac; uterus extends from this point to anterior quarter of segment, not reaching anterior extent of testes; uterine pore absent. Ventral osmoregulatory canal c. 6 in diameter. Gravid segments absent.

Remarks. Otobothrium crenacolle is redescribed from a single specimen here designated as a neotype and five excellently preserved specimens from the type locality and probably from the type host. The host identity of the latter specimens described was given simply as “hammer head shark”, but in the Woods Hole area is almost certainly Sphyrna zygaena (see Compagno 1984, p. 554), the type host of O. crenacolle . The present redescription allows details of the mature segments and armature to be presented for the first time as Linton’s original description was brief and there have been no detailed redescriptions of the adults of the species since.

Linton (1890) originally described O. crenacolle from a hammer-head shark, Sphyrna zygaena , collected at Woods Hole, Massachusetts. Subsequently, he ( Linton 1905, 1907a, b, 1924) reported the same species from Carcharhinus obscurus (Le Sueur, 1818) , C. leucas (Valenciennes, 1839) (= C. platyodon (Poey, 1861)) and Rhizoprionodon terraenovae (Richardson, 1836) (= Scoliodon t.) but did not redescribe the adult. Linton (1901, 1905, 1907a, b, 1910, 1924) also described the plerocercus from numerous species of teleosts from the east coast of North America. The only significant description remains that of the adult made by Linton (1890). Comparison of measurements between Linton's original description and the redescription presented here ( Table 1 ) indicates close agreement. Linton (1890) did not provide details of the number of testes; his figure (Plate 13, fig.9) shows 74 testes compared with 99–178 in the redescription, but his figure is highly schematic and the number of testes shown may not be accurate. In spite of this possible discrepancy, the current redescription closely resembles the original.

In this redescription, the armature is described in detail for the first time; the genitalia are described and the presence of an hermaphroditic duct is established in the type species of the genus. The tentacles of the specimens examined were not fully everted. It was not possible therefore to determine the extent of variation in numbers of hooks in the principal and intercalary rows or to illustrate all views of the tentacle.

No material exists from Linton's original description of the species in 1890. The only extant specimen identified by Linton and derived from the type host, S. zygaena , collected at the type locality, Woods Hole, Massachusetts, USA, is a slide in USNPC (7695) containing several cestodes designated O. crenacolle by Linton (1924). The slide contains a single specimen clearly identifiable as O. crenacolle , as well as three other much smaller specimens which may belong to another species. The additional specimens have much smaller scoleces (250 long) and smaller bulbs (60 long, 30 wide). The tentacles are not everted and therefore their armature cannot be examined in detail. The terminal segments of two specimens have 157 and 139 testes respectively, that is testis numbers equal to or larger than that of specimens clearly identifiable as O. crenacolle . These additional specimens are probably not specimens of O. crenacolle but are not identifiable as any other currently described species. Since no holotype is extant and due to confusion concerning the status of O. crenacolle (see Palm & Overstreet 2000), a neotype has been designated. The specimen comes from the type host ( Sphyrna zygaena ) and from the type locality, Woods Hole, USA, was identified as O. crenacolle by Edwin Linton and conforms with the published description. The designation of the neotype complies with the recommendations of the International Commission of Zoological Nomenclature.

Palm (1995) suggested that O. crenacolle was a synonym of O. cysticum (Mayer, 1842) . Palm & Overstreet (2000) supported this synonymy based on the examination of plerocerci from Peprilus burti Fowler, 1944 , a principal intermediate host. The plerocerci identified by Linton as O. crenacolle were not re-examined as data presented below suggest that species within this group can only be confidently identified on the basis of adults. The proposal by Palm & Overstreet (2000) that O. crenacolle be treated as a synonym of O. cysticum is not consistent with the data presented here.

Otobothrium crenacolle is readily distinguishable from other small species of Otobothrium including O. cysticum by the large bothrial pits measuring approximately 20 µm in internal diameter.

Specimens from Australian and Malaysia varied somewhat in size ( Table 1 ) but generally conformed with the redescription of the species. Given the current state of knowledge, no explanation can be given for the variation observed. It may be that the specimens here identified as O. crenacolle represent one or more very closely related species, but the limited information available provides insubstantial evidence in support of this hypothesis. The records of O. crenacolle presented here substantially extend the host and geographic range of the species.

Linton (1909) also reported O. crenacolle from Carcharhinus leucas , with a single extant specimen collected in the Dry Tortugas, Florida (USNPC 9016). This specimen is a fragment 1.66 mm long. The scolex (270 long) is much shorter than that of O. crenacolle , and in the only complete mature segment, there are approximately 40 testes, with none posterior to the ovary. The specimen is clearly not O. crenacolle but probably belong to O. minutum , a poorly described species purportedly lacking testes posterior to the ovary ( Subhapradha 1955).

Palm (1995) and Palm & Overstreet (2000) also reported the species from Rhizoprionodon acutus . A specimen kindly lent by Dr Palm and now in his collection has small bothria and 76 testes in mature segments. This specimen is not O. crenacolle but is not clearly identifiable with any known species. Examination of various specimens held in collections therefore suggests that additional species related to or formerly confused with O. crenacolle remain to be described.

Figures

FIGURES 1 – 5. Otobothrium crenacolle Linton, 1890 based on specimens in MHNG. 1, Entire mature cestode. 2, Scolex, lateral view. 3, Bulb. 4, Mature segment. 5, Terminal genitalia. Scale bars: Fig. 1, 1.0 mm; Fig. 3, 0.01 mm, Figs. 2, 4, 5, 0.1 mm.

FIGURES 6 – 8. Otobothrium crenacolle Linton, 1890 based on specimens in MHNG. Basal and metabasal armature. 6, Internal surface. 7, External surface. 8, Antibothrial surface. Scale bar: 0.01 mm.

Tables

TABLE 1. Comparison of measurements of the type specimens of Otobothrium crenacolle Linton, 1890 with the redescription from the type locality and specimens from Malaysia and Australia (measurements in µm except for cestode length in mm).

	Linton (1890)	Current redescription	Australian specimens	Malaysian specimens
Length of cestode	10.8–14.0 (11.9, n=4)	13.2–15.9 (14.1, n=5)	3.6–8.5 (5.6, n=5)	4.2–7.0 (5.4, n=5)
Scolex length	360–400 (370, n=4)	385–435 (400, n=5)	420–520 (474, n=5)	260–340 (306, n=5)
Max. scolex width	160–180 (170, n=4)	154–177 (169, n=5)	190–230 (206, n=5)	120–150 (143, n=5)
Pars bothrialis	200–220 (215, n=4)	169–250 (216, n=5)	200–250 (226, n=5)	150–210 (186, n=5)
Bulb length	60–100 (80, n=3)	69–92 (81, n=5)	90–110 (102, n=5)	70–90 (76, n=5)
Bulb width	40–50 (47, n=3)	54–65 (58, n=5)	50–60 (58, n=5)	40–60 (48, n=5)
Diam. of bothrial pit	25	20	25–33 (28, n=5)	25–28 (26, n=5)
Total no. of testes	?74 (from fig.)	118–139 (128, n=5)	98–112 (106, n=5)	101–127 (110, n=3)
No. pre-vaginal		81–106 (90, n=5)	59–77 (67, n=5)	71–88 (77, n=3)
No. pre-ovarian		1–3 (2, n=5)	2–7 (5, n=5)	3–8 (5, n=5)
No. post-ovarian		31–41 (36, n=5)	32–38 (32, n=5)	26–31 (28, n=5)