Benedeniella macrocolpa ( Lühe, 1906 ) Yamaguti, 1963

Whittington, Ian D., 2010, Revision of Benedeniella Johnston, 1929 (Monogenea: Capsalidae), its assignment to Entobdellinae Bychowsky, 1957 and comments on subfamilial composition, Zootaxa 2519, pp. 1-30 : 6-15

publication ID	https://doi.org/ 10.5281/zenodo.196223
DOI	https://doi.org/10.5281/zenodo.6207322
persistent identifier	https://treatment.plazi.org/id/03C11D43-D31D-FFE7-FF7F-43939F9B5655
treatment provided by	Plazi
scientific name	Benedeniella macrocolpa ( Lühe, 1906 ) Yamaguti, 1963
status

Treatment

Benedeniella macrocolpa ( Lühe, 1906) Yamaguti, 1963 View in CoL

( Figs. 1 View FIGURE 1 , 2 View FIGURE 2 , 3 View FIGURE 3 A–B, 4, 5A, 6, 7)

Synonyms: Epibdella (Benedenia) macrocolpa Lühe, 1906 ; Epibdella macrocolpa ( Lühe, 1906) MacCallum, 1927 ; Benedenia (Benedeniella) macrocolpa ( Lühe, 1906) Johnston, 1929 ; Benedenia macrocolpa ( Lühe, 1906) Meserve, 1938 .

Type host: Rhinoptera javanica Müller & Henle (Myliobatidae) , the javanese cownose ray ( Lühe 1906).

Type locality: Kalpitiya, Sri Lanka ( Lühe 1906).

Other published host and locality records: R. javanica, Dutch Bay , Sri Lanka ( Lühe 1906); captive R. javanica in an aquarium at Atlantis The Palm Hotel, Dubai, United Arab Emirates but caught from the wild north of Dubai, Arabian Gulf (present study); R. javanica [but reevaluated and redetermined in the present study as R. neglecta Ogilby ], Moreton Bay (27°25’S, 153°20’E), Queensland, Australia ( Kearn & Whittington 1991, 1992; present study); captive R. neglecta at Reef HQ Aquarium, a public display aquarium in Townsville, Queensland, Australia, but hosts initially collected in a creek flowing into the Ross River, Townsville, Queensland, Australia (present study); R. cf. neglecta (autopsy numbers CMO 3-31, CMO3-48) and Rhinoptera sp. (autopsy number CMO3-43) off Weipa (12°40'S, 141°52'E), Gulf of Carpentaria, Queensland, Australia (present study). Note that CMO3 numbers are unique autopsy identifiers assigned by collectors Professor J. Caira and Dr K. Jensen and can be used to access additional host information at a website dedicated to surveys of elasmobranchs for metazoan parasites at http://web2.uconn.edu/tapeworm/ hosts.php.

Site of infection: Skin according to Lühe (1906); ventral skin ( Kearn & Whittington, 1991, 1992, present study).

Infection details: unknown for specimens from R. javanica from the Arabian Gulf.

In February/ March 1989, 4 specimens of R. neglecta from Moreton Bay, Queensland, Australia were examined (disc width range: 43–100 cm; sex undetermined), 2 of which were infected (disc widths: 43 cm [6 parasites including 2 juveniles], 48 cm [1 juvenile parasite]). Prevalence 50%; infection intensity, 1–6 (3.5); these rays were dead for nearly 2 h by time of dissection and had live parasites on the ventral skin.

In March 1991, 2 specimens of R. neglecta from Moreton Bay, Queensland, Australia were both infected (disc widths: 52 cm [1 parasite], 62 cm [4 parasites]; host sex undetermined). Prevalence 100%; infection intensity, 1–4 (2.5); these rays were dead for nearly 3 h by time of dissection and had living parasites on the ventral skin.

Infection details unknown for material from captive R. neglecta from Reef HQ Aquarium, Townsville, Queensland, Australia.

In June 2003, 2 male specimens of R. cf. neglecta (CMO3-31, CMO3-48) off Weipa, Gulf of Carpentaria, Queensland, Australia were infected (disc widths: CMO 3–31, 131 cm [4 parasites including 1 juvenile], CMO 3–48, 134 cm [5 adult parasites]). Prevalence 100%; infection intensity 4–5 (4.5).

In June 2003, 1 male specimen of Rhinoptera sp. (CMO3-43) off Weipa, Gulf of Carpentaria, Queensland, Australia was infected (disc width: 127 cm [8 parasites including 3 juveniles].

Material deposited: BMNH 2010.4.16.1–3 (3 specimens, 3 slides), SAMA AHC 29900 (4 specimens, 4 slides), USNPC No. 103009 – 103011 (3 specimens, 3 slides) ex captive specimens of R. javanica from an aquarium at Atlantis The Palm Hotel, Dubai, United Arab Emirates (original source, DBV); BMNH 2010.4.16.4–5 (2 specimens, 2 slides), SAMA AHC 29901 (3 specimens, 3 slides), USNPC No. 103012 – 103013 (2 specimens, 2 slides) ex R. neglecta collected in 1989, SAMA AHC 29902 (1 specimen, 1 slide), 2 sectioned specimens (referred to by Kearn & Whittington 1992 but not deposited until now) SAMA AHC 29903 (15 slides of oblique 6 µm sections), SAMA AHC 29904 (9 slides of oblique 6 µm sections) ex R. neglecta collected in March 1991, Moreton Bay (27°25’S, 153°20’E), Queensland, Australia; BMNH 2010.4.16.6-8 (3 specimens, 3 slides), SAMA AHC 29905 (4 specimens, 4 slides), USNPC No. 103014 – 103016 (3 specimens, 3 slides) ex R. neglecta ex Reef HQ Aquarium, Townsville, Queensland, Australia; BMNH 2010.4.16.9 (1 specimen, 1 slide), SAMA AHC 29906 (2 specimens, 2 slides), USNPC No. 103017 (1 specimen) ex R. cf. neglecta (CMO 3-31) off Weipa (12°40'S, 141°52'E), Gulf of Carpentaria, Queensland, Australia; BMNH 2010.4.16.10–11 (2 specimens, 2 slides), SAMA AHC 29907 (3 specimens, 3 slides), USNPC No. 103018 (2 specimens, 2 slides) ex Rhinoptera sp. (CMO3-43) off Weipa (12°40'S, 141°52'E), Gulf of Carpentaria, Queensland, Australia.

Redescription: Based on several live juvenile and adult specimens from Moreton Bay, Queensland, 20 flattened wholemounted adults, 15 flattened wholemounted juveniles, two series of oblique sections of two adults and one adult specimen processed for SEM from Australia and 10 wholemounted adults from the Arabian Gulf. Measurements from 20 flattened wholemounted specimens (all sexually mature) from Australia, except hooklets measured in 10 flattened wholemounted juvenile specimens from Australia; length of everted cirrus measured in four wholemounts from the Arabian Gulf only. Body broadly oval ( Fig. 1 View FIGURE 1 ). Total length (including haptor) and maximum breadth (at level of testes): 4.13–10.67 (7.18, n = 20) x 2.5–6.54 (4.58, n = 20) mm. Haptor 1.29–2.89 (2.21, n = 20) x 1.32–2.78 (2.06, n = 20) mm; wider anteriorly, tapering posteriorly ( Fig. 1 View FIGURE 1 ). Accessory sclerites large, 301–582 (459, n = 40) long, near haptor centre; shaped like spear-head; proximal end with notch ( Figs 1 View FIGURE 1 , 2 View FIGURE 2 A, 3A); distal tips pointed, directed anteriorly ( Fig. 1 View FIGURE 1 ). Anterior hamuli large, stout, strongly recurved distally, 373–839 (665, n = 40) long, with hooked distal tips ( Fig. 2 View FIGURE 2 B). Hooked distal tips of one or both anterior hamuli broken off and missing in 13 mounted specimens from Townsville and Weipa, Queensland, Australia, leaving blunt tips. Posterior hamuli relatively small, 53–84 (74, n = 33) long, slender with hooked distal tips ( Fig. 2 View FIGURE 2 C); position at haptor periphery indicated by marginal indentation ( Fig. 1 View FIGURE 1 ). Hooklets 11–15 (13, n = 45) long ( Fig. 2 View FIGURE 2 D); positions on posterior and posterolateral borders of haptor indicated by marginal indentations ( Fig. 1 View FIGURE 1 ). Tendons conspicuous, travelling posteriorly from extrinsic muscles associated with haptor on each side of body; passing through notch at proximal ends of accessory sclerites before dividing, with part attaching to proximal ends of anterior hamuli and part attaching to ventral haptor tissue ( Figs 1 View FIGURE 1 , 2 View FIGURE 2 E, 3A). Marginal valve running anteriorly from position of hooklets IV on each side of haptor extending to anteriormost region of haptor; wider anteriorly; absence on posteriormost part of haptor (e.g. Fig. 1 View FIGURE 1 ) due to narrow width and damage. Ventral haptor surface apapillate. Pair of conical structures dorsal to haptor near peduncle observed with SEM ( Fig. 4 View FIGURE 4 B, C); less apparent in wholemounts but visible if specimens viewed with dorsal surface uppermost (e.g. Fig. 5 View FIGURE 5 A).

Anterior attachment organs ventral, almost circular, saucer-like discs, 467–1,350 (872, n = 38) x 603–1,251 (868, n = 40); ventral anterolateral region bearing conspicuous, complete grooves ( Figs 1 View FIGURE 1 , 3 View FIGURE 3 B) of variable number, 11–28 (18, n = 55). Number of grooves in juvenile individuals similar to adults. In addition to complete grooves, 0–9 (3, n = 28) incomplete grooves present, of different lengths, occupying positions between complete grooves ( Fig. 3 View FIGURE 3 B). Pair of rounded papillae (sense organs?) at anterior extremity of body proper between anterior attachment organs ( Figs 1 View FIGURE 1 , 3 View FIGURE 3 B). Additional pair of tapering papillae resembling horns located dorsally, one on each anterior attachment organ near junction with body ( Figs 1 View FIGURE 1 , 4 View FIGURE 4 A, 5A); affinity for carmine in stained specimens. Eyes two pairs, pigment-shielded, dorsal, anterior to pharynx. Pharynx conspicuous, 387–1,106 (717, n = 20) x 404–976 (693, n = 20); intrinsic gland cells numerous posteriorly, staining with Ehrlich's haematoxylin and carmine or conspicuously granular in unstained specimens. Intestinal caeca branching extensively in body proper, coextensive with and mostly obscured by vitellarium; unclear whether gut caeca confluent posteriorly. Excretory bladders mostly conspicuous, each opening dorsally at level of posterior region of pharynx on distinct excretory papilla ( Figs 1 View FIGURE 1 , 4 View FIGURE 4 A, 5A), with affinity for carmine.

Testes ovoid, juxtaposed, 491–1,327 (972, n = 32) x 395–1,276 (894, n = 32); penetrated by many dorsoventral muscle bundles ( Fig. 1 View FIGURE 1 ). Glands of Goto absent in juvenile and adult specimens. Vasa efferentia short (not drawn) uniting immediately posterior to germarium. Vas deferens travelling to left of germarium, passing dorsal to transverse vitelline ducts and proximal region of vagina, then becoming intensely convoluted, occupying space within curve formed by sac of male copulatory organ (= cirrus) posterior to ootype ( Figs 1 View FIGURE 1 , 6 View FIGURE 6 ); breaching muscular wall of cirrus sac dorsally at anterior level of ootype chamber. Inside cirrus sac, vas deferens narrows, following winding path dorsally to proximal end, then returning ventrally to base of cirrus ( Fig. 6 View FIGURE 6 ). No evidence for widening of vas deferens or presence of sperm-filled reservoir inside cirrus sac, but structure and arrangement difficult to determine, even in sections, due to complexity and convolutions within cirrus sac. Male accessory gland reservoir single, lying ventrally in cirrus sac; source of male accessory secretion not identified; no ducts observed penetrating proximal region of cirrus sac. Cirrus sac wall provided with muscle fibres (not shown); length and extent of curvature of cirrus sac increasing with increase in size of parasite; in juvenile and some small adult specimens, distal portion lying diagonally in body posterior to pharynx with proximal part curving medianly immediately anterior to germarium and/or testes ( Fig. 7 View FIGURE 7 A); in most large specimens, proximal region of cirrus sac may curve anteriorly, dorsal to ootype chamber, forming a complete loop enclosing common vitelline duct, oviduct, ovo-vitelline duct, ootype and convolutions of vas deferens ( Fig. 7 View FIGURE 7 B). Distal duct from male accessory gland reservoir and distal part of vas deferens uniting near base of cirrus at anterior level of ootype chamber ( Figs 1 View FIGURE 1 , 6 View FIGURE 6 ). Cirrus long, sinuous, often twisted on itself, running anterolaterally inside terminal male genital duct, ventral to separate uterus, opening submarginally, slightly dorsal, on left side of body via common genital pore on short genital papilla at a level anterior to pharynx close to posterior margin of left anterior attachment organ ( Figs 1 View FIGURE 1 , 6 View FIGURE 6 ). Cirrus capable of eversion outside animal to length of 2.6–4.1 (3.5, n = 4 measured along curves from wholemounted adult specimens from Arabian Gulf) mm.

Germarium immediately pretesticular with extensive, centrally located fertilisation chamber ventrally at mid-line ( Figs 1 View FIGURE 1 , 6 View FIGURE 6 ), containing ripe oocytes. Oviduct long, narrowing immediately anterior to transverse vitelline duct, convoluted, travelling anteriorly, joining relatively long common vitelline duct from dorsal part of vitelline reservoir to form short ovo-vitelline duct. Numerous fine gland ducts entering ovo-vitelline duct at base of proximal region of ootype ( Fig. 6 View FIGURE 6 ); many small gland cells (not shown) located in curve of cirrus sac, right of oviduct. Ootype with convoluted proximal duct leading to tetrahedral-shaped chamber at level of excretory bladders, leading into uterus. Uterus long, following parallel course dorsal to terminal male genital duct, uniting near base of genital papilla ( Fig. 6 View FIGURE 6 ; see also Kearn & Whittington 1992). Common genital duct short, opening dorsomarginally at common genital pore at distal end of short genital papilla ( Figs 1 View FIGURE 1 , 4 View FIGURE 4 A, 6).

Vitelline reservoir ventral, curving anteromedianly, near proximal end of cirrus sac. Vagina exceedingly long, 2.1–11 (6.6, n = 13, measured along curves) mm; originating proximally via narrow duct from left dorsal margin of vitelline reservoir. No seminal receptacles or proximal specialisations. Vagina following path posteriorly to a level well behind testes before turning anteriorly through 180°, passing ventral to left excretory bladder, then running parallel, just posterior to terminal male genital duct and uterus, to open dorsomarginally, just posterior to common genital papilla ( Figs 1 View FIGURE 1 , 6 View FIGURE 6 ). Vitellarium follicular, extending from between anterior attachment organs almost to posterior extremity of body proper, coextensive with intestinal caeca ( Fig. 1 View FIGURE 1 ). Free eggs not observed; in some mounted specimens, eggs observed in ootype, with tetrahedral shape and appendage; no egg measurements made due to distortion during specimen processing.

Remarks: Live specimens of B. macrocolpa from R. neglecta collected from Moreton Bay, Queensland, Australia were apparently healthy. They attached to the bottom of glass Petri dishes containing FSW, displayed leech-like locomotion by alternately attaching the haptor and anterior attachment organs (e.g. see Whittington et al. 2000) and also exhibited characteristic undulating movements of the body while attached by the haptor. For the capsalid Entobdella soleae, Kearn (1962) has demonstrated that these regular undulatory motions probably aid respiration of the parasite. Living specimens of B. macrocolpa attached to glass dishes failed to lay any eggs during periods of up to 7 h.

The anatomy of B. macrocolpa redescribed here is consistent in most respects with that presented by Lühe (1906). The only major difference relates to the arrangement of the terminal female and male genital systems. Lühe (1906) described a short uterus that opened into a long common genital duct. The present study, however, confirms the view of Kearn & Whittington (1992) that the uterus of B. macrocolpa is, in fact, long and runs parallel with and dorsal to the separate elongate terminal male genital duct. The female and male systems unite only distally near the base of a short common genital papilla to form a short common genital duct which opens dorsally ( Figs 1 View FIGURE 1 , 5 View FIGURE 5 A, 6).

Additional anatomical features emphasised in this redescription of B. macrocolpa relate to the presence and path of conspicuous tendons from extrinsic muscles in the body associated with the haptor and a series of 11–28 complete roughly parallel, ventral, narrow grooves on the anterolateral margin of each anterior attachment organ. In some specimens, there may be some incomplete grooves between the complete grooves. The grooves on the anterior attachment organs of B. macrocolpa resemble similar structures described by Hargis (1955) on the anterior attachment organs of B. posterocolpa and their presence is confirmed in the redescription below. The route of the tendons in the haptor of B. macrocolpa and their attachment mostly to the proximal ends of the anterior hamuli is shared by B. posterocolpa (see below), Entobdella species (e.g. in E. soleae , see Kearn 1964) and some Neoentobdella species (see Kearn & Whittington 2005).

This redescription of B. macrocolpa has also identified dorsal structures associated, in anterior to posterior succession, with the anterior attachment organs, common genital pore, excretory bladders and at the junction of the body with the haptor. The anteriormost tapering papillae are horn-like and were also described by McMahon (1963) for B. posterocolpa (see below). With the exception of the common genital papilla, all dorsal structures identified here for B. macrocolpa have also been identified in the present study for B. posterocolpa (see Fig. 5 View FIGURE 5 and below). These characters are included in the amended generic diagnosis above.