Prochristianella jensenae, Schaeffner, Bjoern C. & Beveridge, Ian, 2012

Schaeffner, Bjoern C. & Beveridge, Ian, 2012, Prochristianella Dollfus, 1946 (Trypanorhyncha: Eutetrarhynchidae) from elasmobranchs off Borneo and Australia, including new records and the description of four new species, Zootaxa 3505, pp. 1-25 : 7-14

Prochristianella jensenae n. sp.

( Figs 4–6 )

Material examined: 83 whole-mounts, 3 specimens used for SEM, tentacles detached from 1 specimen.

Type-host: Pastinachus solocirostris Last, Manjaji & Yearsley, Roughnose stingray ( Rajiformes : Dasyatidae ) (BO-164, BO-165, BO-177, BO-256, BO-267, KA-44, KA-148).

Additional hosts: Pastinachus atrus (Macleay) , Eastern cowtail stingray ( Rajiformes : Dasyatidae ) (KA-32), Pastinachus gracilicaudus Last & Manjaji-Matsumoto, Narrowtail stingray ( Rajiformes : Dasyatidae ) (BO-99), Himantura uarnak (Gmelin) , Honeycomb stingray ( Rajiformes : Dasyatidae ), Rhinoptera neglecta Ogilby , Australian cownose ray ( Rajiformes : Myliobatidae ).

Type-locality: Sematan, Sarawak, Malaysia.

Additional localities: Mukah, Sarawak and Kampung Tetabuan, Sabah, Malaysia; Muara Pasir and Sei Kerbau, East Kalimantan, and Singkawang, West Kalimantan, Indonesia; Weipa, Queensland and Nickol Bay, Western Australia, Australia.

Site of infection: Spiral intestine.

Deposited specimens: Holotype ( MZUM No 2012.04). Paratypes in ( MZUM Nos 2012.05–08; MZB Nos Ca 168–175; USNPC Nos 105181–105182; LRP Nos 7843–7849; and SAM Nos AHC 35408–35450).

Etymology: This species is dedicated to Dr. Kirsten Jensen for her significant sampling efforts in Borneo and Australia.

Description: Cestodes, small, euapolytic, 2.3–5.9 (3.3 ± 0.9; n = 18) mm long, with 5–7 (6 ± 1; n = 10) segments ( Figs. 4 A, 6A). Scolex acraspedote, 950–1,620 (1,220 ± 170; n = 18) long, 150–190 (180 ± 20; n = 6) wide at level of bothria ( Fig. 4 B); pars bothrialis 170–280 (230 ± 30; n = 19) long; two oval bothria, with free posterior margins, notched posteriorly, with internal V-shaped ridge ( Figs. 4 B, 6B); pars vaginalis 530–1,080 (760 ± 160; n = 18) long; tentacle sheaths sinuous; pars bulbosa 370–520 (450 ± 40; n = 18) long, 140–200 (170 ± 20; n = 19) wide; prebulbar organs present; bulbs elongate, thin-walled, 360–500 (420 ± 30; n = 19) long, 50–80 (60 ± 10; n = 19) wide ( Fig. 4 B, C); bulb width: length ratio 1.0: 5.1–9.2 (7.3 ± 1.2; n = 19); retractor muscle originates at base of bulb; gland-cells within bulb absent ( Fig. 4 B, C); scolex ratio (pars bothrialis: pars vaginalis: pars bulbosa) 1.0: 2.3–5.2: 1.8–2.6 (1.0: 3.4 ± 0.7: 2.0 ± 0.2; n = 18). Pars postbulbosa short, 50–110 (80 ± 20; n = 7) long.

Everted tentacles c. 410 (n = 1) long; tentacle diameter 40–45 (43 ± 2; n = 5) at base, 30–40 (35 ± 5; n = 5) in metabasal region, 25–33 (29 ± 4; n = 5) in distal region. Armature heteroacanthous, heteromorphous; hooks hollow ( Figs. 5 A–D, 6C, F). Metabasal armature arranged in ascending half-spiral rows; hook rows consist of 6 hooks, begin on bothrial surface of tentacle ( Fig. 5 D), terminate on antibothrial surface ( Fig. 5 B, C); hook files 1 and 1’ slightly spaced ( Figs. 5 D, 6C); hooks increase in size and then decrease towards antibothrial surface ( Figs. 5 A–D, 6F); hooks 1(1’) uncinate, 8–11 (9 ± 1; n = 7) long, base 5–8 (6 ± 1; n = 7) long; hooks 2(2’) larger, falcate with slightly recurved tip, 12–14 (13 ± 1; n = 7) long, base 4–5 (4 ± 1; n = 7) long; hooks 3(3’) falcate with slightly recurved tip, 11–14 (12 ± 1; n = 8) long, base 3–4 (4 ± 1; n = 8) long; hooks 4(4’) falcate, smaller, 9–11 (11 ± 1; n = 8) long, base 2–3 (2 ± 1; n = 8) long; hooks 5(5’) falcate, smaller, 9–10 (9; n = 8) long, base 2–3 (2; n = 8) long; hooks 6(6’) falcate, 8–10 (9 ± 1; n = 8) long, base 1–2 (1; n = 8) long.

Basal armature distinct, basal swelling absent ( Figs. 5 A, C, 6E); largest hooks at base uncinate, solid, 9–12 (11 ± 1; n = 6) long, base 5–7 (6 ± 1; n = 6) long; billhooks anterior to base of tentacles hollow, erect, 8–9 (9 ± 1; n = 13) long; base inconspicuous, 2–3 (2; n = 13) long ( Figs. 5 A, C, 6D, E), flattened in antero-posterior plane ( Fig. 6 D), form several rows surrounding tentacle, not intermingled with other hooks.

Segments acraspedote; mature segments longer than wide, 720–2,040 (1,340 ± 360; n = 19) long, 120–250 (180 ± 30; n = 19) wide ( Fig. 4 D); genital pores alternate irregularly, on lateral margins; pore inconspicuous; cirrus sac oval, thick-walled, in mid-line of segment or slightly anterior ( Fig. 4 D, E), 83–125 (103 ± 21; n = 4) long, 48–150 (88 ± 46; n = 4) wide; cirrus unarmed, strongly coiled inside cirrus sac; internal and external seminal vesicles absent. Testes exclusively preovarian, subspherical, in two columns, in single layer, 37–56 (46 ± 6; n = 11) in number, almost same number anterior and posterior to cirrus sac, 16–30 (22 ± 5; n = 11) preporal, 19–28 (23 ± 3; n = 11) postporal, 50–85 (60 ± 9; n = 16) long, 35–50 (39 ± 4; n = 16) wide ( Fig. 4 D). Vagina 15–20 (18 ± 2; n = 4) wide; seminal receptacle between ovarian lobes anterior to ovarian isthmus, oval, 36–43 (39 ± 5; n = 2) long, 26–31 (29 ± 3; n = 2) wide; ovary bilobed in dorso-ventral view; ovarian lobes 250–405 (304 ± 49; n = 12) long, 28–63 (51 ± 12; n = 12) wide ( Fig. 4 D); Mehlis’ gland posterior to ovarian isthmus, 30–40 (34 ± 4; n = 4) in diameter; vitelline follicles circumcortical, 13–20 (16 ± 2; n = 17) in diameter; uterus median, tubular, simple; uterine pore not observed.

Gravid segments longer than wide, 1,210–2,850 (1,860 ± 710; n = 5) long, 310–400 (340 ± 40; n = 5) wide ( Fig. 4 E); uterus saccate, distinctly swollen in region of genital pore; eggs ovoid, thin-shelled, non-operculate, nonembryonated, 21–25 (23 ± 1; n = 40) in diameter.

Remarks: The species described above is allocated to the genus Prochristianella , due to the presence of prebulbar organs and the changes in hook sizes in the metabasal armature, with hooks gradually increasing and then decreasing in size. Specimens of this species can be easily recognized by having characteristic erect, hollow billhooks in the basal armature of each tentacle. Prochristianella jensenae n. sp. represents a unique species within the genus, since it lacks gland-cells within the tentacular bulbs. The presence of gland-cells is one of the defining features for taxa within the Eutetrarhynchoidea Dollfus, 1969 (see Palm 2004). Only two other species within this superfamily, namely Shirleyrhynchus aetobatidis ( Shipley & Hornell, 1906) and Rhinoptericola megacantha Carvajal & Campbell, 1975 , lack gland-cells inside the muscular bulbs (see Beveridge & Campbell 1988, Carvajal & Campbell 1975, Palm 2004). Both species, however, possess a scolex with four oval bothria, a character of the family Rhinoptericolidae Carvajal & Campbell, 1975 to which both species belong. Prochristianella jensenae n. sp. has only two bothria and, thus, represents the first taxon within the Eutetrarhynchidae Guiart, 1927 lacking glandcells. Although allocated within the genus Prochristianella due to apparent similarities, P. jensenae n. sp. differs from all congeners in having a cirrus sac situated at the mid-line of the proglottid, absence of a basal swelling and a large number of testes posterior to the cirrus sac. The most distinctive characteristic, however, are the principle hook rows in the metabasal tentacular armature, which run from the bothrial to the antibothrial surface. This commencement of the principle hook rows on the bothrial surface has also been reported for another species, P. fragilis by Heinz & Dailey (1974). The differences from congeners, however, are not considered to be sufficient to warrant the erection of a new genus. More material preserved in ethanol for molecular studies is needed to clarify the taxonomic placement of P. jensenae n. sp. This species was collected from six localities from Borneo and two localities from northern Australia. Although a huge number of elasmobranch hosts have been collected in waters off Borneo, the present specimens were obtained exclusively from the spiral intestines of three species of the dasyatid genus Pastinachus Rüppell , revealing a high host specificity. However, this high host specificity of P. j e n s e n a e n. sp. in Borneo is considered to be a local phenomenon with host species of other genera being infected outside the Indo- Malayan region.

Prochristianella kostadinovae n. sp. ( Figs 7 & 8 )

Material examined: 11 whole-mounts.

Type-host: Himantura uarnak 2 (sensu Naylor et al. 2012) ( Rajiformes : Dasyatidae ) (CM03-24, CM03-25, CM03-65).

Type-locality: Weipa, Queensland, Australia.

Site of infection: Spiral intestine.

Deposition of specimens: Holotype ( SAM No AHC 35400). Paratypes in ( SAM Nos AHC 35401–35402; LRP Nos 7835–7837; USNPC Nos 105178–105179).

Etymology: This species is dedicated to Dr. Aneta Kostadinova for her contributions to fish parasitology.

Description: Cestodes, small, 4.6–5.6 (5.2 ± 0.3; n = 7) mm long, with 9–10 (9; n = 7) segments. Scolex acraspedote, 1,265–1,590 (1,422 ± 119; n = 7) long, maximum width at level of bothria, 360–400 (375 ± 16; n = 5) wide ( Fig. 7 A, C); pars bothrialis 190–270 (236 ± 28; n = 7) long; two oval bothria, 210–230 (223 ± 12; n = 3) long, 230–300 (263 ± 29; n = 4) wide, with free margins, rims thickened, posteriorly notched, with prominent Vshaped ridge ( Fig. 7 A, C); pars vaginalis 750–1,070 (923 ± 118; n = 7) long; tentacle sheaths sinuous to irregularly coiled ( Fig. 7 A, C); pars bulbosa 470–525 (496 ± 23; n = 7) long, 180–230 (209 ± 17; n = 7) wide; prebulbar organs present, small; bulbs elongate, sinuous, thick-walled, 480–510 (491 ± 10; n = 10) long, 70–90 (76 ± 1; n = 10) wide, reach to pars proliferans ( Fig. 7 C, D); bulb width: length ratio 1.0: 5.4–7.1 (6.5 ± 0.6; n = 10); retractor muscle inserts at base of bulb; gland-cells within bulb present ( Fig. 7 C, D), mostly in posterior third of bulb, in some specimens to anterior end or anterior third of bulb; scolex ratio (pars bothrialis: pars vaginalis: pars bulbosa) 1.0: 3.2–4.7: 1.9–2.5 (1.0: 4.0 ± 0.6: 2.1 ± 0.2; n = 7). Pars postbulbosa absent.

Everted tentacles 590–650 (613 ± 23; n = 6) long; tentacle diameter 23–35 (30 ± 4; n = 6) at base, 35–43 (38 ± 2; n = 8) at level of basal armature, 33–40 (37 ± 2; n = 12) in metabasal region. Armature heteroacanthous, heteromorphous; hooks hollow ( Fig. 8 A–D). Metabasal armature arranged in ascending half-spiral rows; hook rows consist of 10 hooks ( Fig. 8 D), begin on antibothrial surface of tentacle, terminate on bothrial surface ( Fig. 8 A, C); hook files 1 and 1’ separated by prominent space ( Fig. 8 B); hooks 1(1’) uncinate, with elongate base, 16–21 (18 ± 2; n = 8) long, base 13–15 (14 ± 1; n = 8) long; hooks 2(2’) larger, falcate, with slightly recurved tip, 17–21 (19 ± 1; n = 14) long, base 8–10 (9 ± 1; n = 9) long; hooks 3(3’) slightly larger, falcate, with recurved tip, 19–21 (20 ± 1; n = 8) long, base 7–10 (8 ± 1; n = 8) long; hooks 4(4’) smaller, falcate, 9–13 (11 ± 1; n = 12) long, base 2–4 (3 ± 1; n = 10) long; hooks 5(5’) larger, falcate, 17–20 (18 ± 1; n = 10) long, base 3–5 (4 ± 1; n = 10) long; hooks 6(6’) smaller, falcate, 6–9 (8 ± 1; n = 12) long, base 2–5 (3 ± 1; n = 12) long; hooks 7(7’)–10(10’) tiny, falcate, 3–5 (4 ± 1; n = 17) long, base 2–3 (2; n = 17) long.

Characteristic basal armature present ( Fig. 8 A); basal hooks of first two rows not enlarged, 5–6 (6 ± 1; n = 4) long, base 4–5 (5 ± 1; n = 2) long; basal swelling weakly developed, with 5 rows of billhooks; billhooks increase slightly in size towards bothrial surface; largest billhooks on bothrial surface, 5–6 (6 ± 1; n = 9) long, base 1–2 (2; n = 9) long; first two rows of hooks on antibothrial surface of basal swelling spiniform, 5–7 (6 ± 1; n = 6) long, base 1 (n = 5) long; become falcate with recurved tips at hook rows 7–9, 5–7 (6 ± 1; n = 5) long, base 1–2 (1; n = 4) long; transition to metabasal armature occurs at row 11 ( Fig. 8 A).

Segments acraspedote; first mature segments slightly elongate, 120–210 (151 ± 34; n = 6) long, 110–160 (133 ± 19; n = 6) wide; late mature segments elongate, 1,310–1,545 (1,397 ± 80; n = 6) long, 170–235 (197 ± 24; n = 6) wide ( Fig. 7 A, B); genital pores alternate irregularly, on lateral margins, in posterior half of segment ( Fig. 7 A, B); pore inconspicuous; cirrus sac sub-circular, thick-walled, 75–110 (93 ± 13; n = 6) long, 90–128 (105 ± 13; n = 6) wide ( Fig. 7 B); cirrus unarmed; internal and external seminal vesicles absent. Testes preovarian, subspherical, 58–70 (66 ± 4; n = 12) long, 33–45 (39 ± 5; n = 12) wide, in two longitudinal columns, in two layers; layers of testes directly above each other in dorso-ventral view ( Fig. 7 B); testes 58–73 (65 ± 5; n = 9) in number, 42–60 (51 ± 5; n = 9) preporal, 11–17 (14 ± 2; n = 9) postporal. Vagina c. 15 (n = 1) wide; seminal receptacle not observed; ovary bilobed in dorso-ventral view; ovarian lobes 120–195 (155 ± 22; n = 12) long, 38–65 (52 ± 9; n = 12) wide ( Fig. 7 B); Mehlis’ gland between posterior parts of ovarian lobes, 55–68 (59 ± 5; n = 6) in diameter; vitelline follicles circumcortical, 30–38 (33 ± 2; n = 10) long, 13–15 (15 ± 1; n = 10) wide in mature segments, 35–43 (39 ± 2; n = 10) long, 18–20 (18 ± 1; n = 10) wide in late mature segments; uterus median, tubular, simple; uterine pore not observed.

Gravid segments not present.

Remarks: This species possesses a slender, acraspedote scolex, a characteristic basal armature, a heteroacanthous metabasal armature with widely separated hooks 1(1’) and hooks of each principle row first increasing and then decreasing in size. It can, thus, be allocated to the genus Prochristianella . With rows of billhooks on the basal swelling of each tentacle and the absence of microscopically visible microtriches on the scolex, this species is closely related to P. aciculata , P. butlerae , P. mooreae and P. odonoghuei . In contrast to these species, P. kostadinovae n. sp. possesses a metabasal tentacular armature with hooks 4(4’) much smaller than neighbouring hooks 3(3’) and 5(5’). Prochristianella aciculata is the only other species with a similar pattern in its metabasal oncotaxy. In the latter species, however, the typical increase and subsequent decrease in hook sizes along the principle rows is interrupted by smaller hooks 5(5’). Prochristianella kostadinovae n. sp. furthermore differs from P. aciculata in having a larger scolex and larger bulbs, a different number and shape of hooks in the metabasal armature and a complete absence of enlarged hooks at the base of each tentacle. Therefore, we consider P. kostadinovae n. sp. to represent a species new to science. The present specimens were obtained from a single locality in northern Australia and from the spiral intestines of three specimens of H. uarnak 2 (sensu Naylor et al. 2012). We, therefore, assume P. kostadinovae n. sp. to be a highly host specific parasite from northern Australian waters.

Figures

FIGURE 4. Prochristianella jensenae n. sp. from Pastinachus solocirostris. A. Complete specimen. B. Scolex. C. Bulb; note absence of gland-cells. D. Mature segment. E. Gravid segment. Abbreviations: cs, cirrus sac; isv, internal seminal vesicle; mg, Mehlis’ gland; ov, ovary; rm, retractor muscle; t, testis; ut, uterus; vit, vitelline follicle.

FIGURE 5. Prochristianella jensenae n. sp. from Pastinachus gracilicaudus (A, D) and P. solocirostris (B, C). Tentacular armature. A. Basal and metabasal regions, internal surface. B. Metabasal region, antibothrial surface. C. Basal and metabasal regions, antibothrial surface. D. Basal and metabasal regions, bothrial surface.

FIGURE 6. Prochristianella jensenae n. sp. from Pastinachus solocirostris. Scanning electron micrographs. A. Complete specimen. B. Scolex in lateral view. C. Tentacular armature; metabasal region, bothrial surface. D. Billhooks in lateral (left) and dorso-ventral (right) views. E. Tentacular armature, basal region, internal surface; note erect billhook. F. Tentacular armature, metabasal region, external surface.

FIGURE 7. Prochristianella kostadinovae n. sp. from Himantura uarnak 2 (sensu Naylor et al. 2012). A. Partial specimen. B. Mature segment. C. Scolex. D. Bulb. Abbreviations: cs, cirrus sac; gc, gland-cells; mg, Mehlis’ gland; ov, ovary; rm, retractor muscle; t, testis; vit, vitelline follicle.

FIGURE 8. Prochristianella kostadinovae n. sp. from Himantura uarnak 2 (sensu Naylor et al. 2012). Tentacular armature. A. Basal and metabasal regions, external surface. B. Basal and metabasal regions, antibothrial surface. C. Basal and metabasal regions, bothrial surface; note opposing surface to (B) of the same tentacle. D. Outlines of metabasal hooks.