Entobdella hippoglossi ( Müller, 1776 ) Blainville, 1818

Kearn, Graham C., Whittington, Ian D. & Evans-Gowing, Richard, 2007, A revision of Entobdella Blainville in Lamarck, 1818, with special emphasis on the nominal (type) species “ Entobdella hippoglossi (Müller, 1776) Blainville, 1818 ” (Monogenea: Capsalidae: Entobdellinae) from teleost flatfishes, with descriptions of three new species and a new genus, Zootaxa 1659, pp. 1-54 : 41-44

Entobdella hippoglossi ( Müller, 1776) Blainville, 1818

( Figs. 1, 3, 7, 8, 15A, 16, 32–34)

(This taxon has been referred to throughout this paper as “ E. hippoglossi type 1”)

[syn. Tertia pediculorum species Baster, 1759 (see Comments below); Hirudo hippoglossi Müller, 1776 ; Phylline hippoglossi ( Müller, 1776) Oken, 1815 ; Epibdella hippoglossi ( Müller, 1776) Blainville, 1828 ; Epibdella sp. of Krøyer, 1843 – 45; Tristoma hamatum Rathke, 1843 ; Epibdella sp. of Van Beneden, 1852; Nitzschia hippoglossi ( Müller, 1776) Taschenberg, 1878 ; Phyllonella hippoglossi ( Müller, 1776) Goto, 1900 ; Epibdella (Phylline) hippoglossi ( Müller, 1776) Monticelli, 1902 ; Epibdella hippoglossi ( Müller, 1776) Cooper, 1921 ; Entobdella (Entobdella) hippoglossi ( Müller, 1776) Johnston, 1929 ; Entobdella curvunca Ronald, 1957 (see below); “ Entobdella hippoglossi type 1” (present study)].

Type host and locality: Atlantic halibut, Hippoglossus hippoglossus (Linnaeus, 1758) ( Pleuronectiformes : Pleuronectidae ). According to Brinkmann (1952b, p. 12), Müller did not mention where the hosts of E. hippoglossi were captured and concluded that “we cannot decide whether they had been collected in Danish or in Norwegian waters”. However, it is necessary to designate a neotype for E. hippoglossi (see below) and according to the International Code of Zoological Nomenclature ( ICZN) (1999), Article 76.3, “the place of origin of the neotype becomes the type locality of the nominal species group taxon, despite any previously published statement of the type locality”. The neotype we have designated was collected by Dr A. Shinn ( Table 1) from a captive halibut caught in the North Atlantic Ocean and held at the Marine Environmental Research Station of the University of Stirling at Machrihanish, Scotland (see Materials and methods).

Other records: Lawler (1981, table 68) gives a comprehensive list of other localities on H. hippoglossus , including widely scattered sites in the North Atlantic Ocean (Scandinavia, Iceland, Greenland and the Gulf of St Lawrence, Canada). The following have also been recorded as hosts: turbot, Psetta maxima (Linnaeus, 1758) ( Pleuronectiformes : Scophthalmidae ), North Sea (authority given as Möbius, 1874 in Lawler 1981); “flétan” (halibut) and Rhombus maximus (= Psetta maxima ), “French waters” (Froissant 1930 in Lawler 1981); gills of “a member of the Gadidae ”, Labrador (Canavan 1934 in Lawler 1981); Greenland halibut, Reinhardtius hippoglossoides (Walbaum, 1792) ( Pleuronectiformes : Pleuronectidae ), North Atlantic Ocean ( Boje et al. 1997) (see Comments below). All of these records require confirmation, especially in view of our discovery that 2 closely related parasite species ( E. hippoglossi and a new species described below) occur on H. hippoglossus .

Site on host: Skin. Parasites collected by Mamaev (1965) from the gills of A. stomias caught in the Bering Sea were identified as Entobdella hippoglossi (see below) but seem more likely to be B. pugetensis (see above). According to Lawler (1981), Müller (1776) did not mention the host species or the location of the parasite on the host, but Müller’s account in Latin includes the phrase “In cute Pleuronectis Hippoglossi ”, indicating that the parasite was found on the skin of what is now the pleuronectid Hippoglossus hippoglossus . Van Beneden (1858) reported the parasite on the lower surface (“la face blanche”) of Pleuronectes (= Hippoglossus ) hippoglossus .

Neotype: BMNH accession No. 2007.4.26.1 (1 slide). Specimen donated by Dr A. Shinn (see Table 1). We establish a neotype because no name-bearing type specimen is known to exist and because we found a second closely related species (described below) on the same host species, Hippoglossus hippoglossus . Prior to now, this second species was not recognised and was considered to be E. hippoglossi . A neotype is therefore designated with the express purpose of clarifying the taxonomic status of parasites of H. hippoglossus , as recommended by the ICZN (4 th edition, 1999, Article 75). The characters differentiating E. hippoglossi from the second species are given below. The neotype is consistent with early descriptions of E. hippoglossi by Müller (1776) and Van Beneden (1858), but these descriptions make no reference to type specimens.

Voucher specimens: 2 adult specimens from captive halibut originally caught in the North Atlantic Ocean , donated by Dr A. Shinn (see Table 1) ( BMNH Nos. 2007.4.26.2-3, 2 slides). One adult specimen from captive halibut originally caught in the North Atlantic Ocean, donated by Dr A. Shinn ( SAMA AHC No. 29193, 1 slide) (see Table 1). Two adult specimens from Faroe Bank (see Table 1) ( BMNH Nos. 2007.4.26.4- 5, 2 slides). One adult specimen from Faroe Bank (see Table 1) ( SAMA AHC 29194, 1 slide). One adult specimen from a captive fish from Lowestoft Fisheries Laboratory ( BMNH No. 2007.4.26.6, 1 slide). One adult specimen from Bergen, Norway (unknown source) ( BMNH No. 2007.4.26.7, 1 slide). One adult specimen from Dr H.H. Williams (see Table 1). ( BMNH No 2007.4.26.8, 1 slide). One immature specimen from captive halibut originally caught in the North Atlantic Ocean, donated by Dr A. Shinn (see Table 1) ( BMNH No. 2007.4.26.9, 1 slide) .

Specimens studied: 10 adult parasites from H. hippoglossus from various sources; 1 immature parasite donated by Dr A. Shinn (see above and Table 1).

Redescription ( Fig. 32): Dimensions of adult parasites; total length 1.288 (0.667 – 1.599) cm (n = 10); body width 6.483 (2.860 – 8.905) mm (n = 10); haptor length and breadth 3987 (2166 – 5505) and 4162 (1985 – 5625) respectively (n = 10); accessory sclerite length 567 (364 – 882) (n = 17); anterior hamulus length 970 (563 – 1396) (n = 20); posterior hamulus length 184 (176 – 195) (n = 3); pharynx length and breadth 675 (416 – 875) and 874 (612 – 1213) respectively (n = 9); testis length and breadth 1343 (688 – 1715) and 1106 (688 – 1474) respectively (n = 20). Anatomy as described by Van Beneden (1858) with the following additional features: subdivision of each anterior adhesive pad into 3 areas visible with scanning electron microscope (SEM) and in some specimens with light microscope. Vaginal aperture on ventral surface small, hard to resolve with light microscope, opening into narrow, relatively straight, thin-walled entrance tube, 4 – 7 in diameter, 60 – 85 long ( Figs. 7, 8). This leads to equally narrow, thick-walled tube, 50 – 66 long, following winding route; wall has affinity for toluidine blue in resin sections. This communicates with main vagina, a tight coiled tube occupying a long narrow column running diagonally across body, roughly parallel with female reproductive tract (oviduct, ootype, uterus) to open proximally into vitelline reservoir ( Fig. 3), not into seminal receptacle as stated by Klassen et al. (1989). Seminal receptacles numerous (4 – 7, possibly more; Fig. 1), not a single receptacle as stated by Klassen et al. (1989). Papillae on haptor relatively few in number [45 (33 – 59) papillae per mm 2 (n = 8)], ranging in diameter from 30 – 125 and regularly exceeding 100. Papillae with conspicuous fleshy apical protuberances, some of which have more than 1 lobe ( Figs. 16, 32C,D); this feature visible in immature specimen ( Fig. 32B). Papillae confined to posterior two-thirds of haptor and, as described by Van Beneden (1858), arranged in radial rows in lateral regions ( Fig. 32A). Eyes conspicuous.

Dimensions of immature specimen (BMNH No.: 2007.4.26.9) as follows: total length 4777; body width 2542; haptor length and breadth equal, measuring 1940; accessory sclerite lengths 331/300; anterior hamulus lengths 512/528; posterior hamulus lengths 135/140; pharynx length and breadth 250 and 425 respectively; length and breadth of testes 613 x 500 and 613 x 488 respectively.

Differential diagnosis: Large, frequently> 1 cm in total length. Similar to a newly described species (see description below) found on lower surface of Pacific halibut ( H. stenolepis ), but E. hippoglossi has fewer papillae on ventral surface of haptor [45 (33 – 59) per mm 2 compared with 75 (59 – 97) per mm 2] and papillae of E. hippoglossi are bigger (regularly> 100 in diameter compared with <70), with conspicuous fleshy apical lobes occasionally divided into 2, 3 or 4 sub-lobes. E. hippoglossi shares its host with another closely related, newly described species (see description below) but is readily distinguished by the following features: 1) inconspicuous vaginal opening, lacking closely associated circularly arranged sub-tegumental fibres; 2) smaller number of papillae on ventral surface of haptor [45 (33 – 59) per mm 2 compared with 129 (105 – 156) per mm 2]; 3) papillae large, diameter regularly>100, compared with 20 – 95; 4) papillae do not extend anterior to peduncular junction and arranged in conspicuous radial rows lateral to median sclerites; 5) papillae frequently have fleshy apical lobes, which may be divided into 2, 3 or 4 sub-lobes. On skin of Atlantic halibut, H. hippoglossus .

Comments. Baster (1759) is quoted as the first record of this parasite (as Tertia pediculorum species) on the halibut by Van Beneden (1858). Van Beneden commented as follows on Baster’s report: “C’est Baster, le premier, qui fait mention de ce parasite de l’hippoglosse; mais, comme il lui est arrivé souvent, Baster a pris la grande ventouse postérieure pour la tête, et il cru devoir le rapprocher des Lernéens de Linné.” Presumably Van Beneden regarded Baster’s description as inadequate to establish the new species since he attributed the parasite to Müller (1776). However, there is no statement as to why Müller was selected as the authority and Van Beneden goes on to state: “En somme, il n’y a que Baster, O. -F. Müller et Rathke qui aient observé cet animal, et eux seuls en ont donné une figure originale.” Susequent authors (e.g. Sproston 1946, Yamaguti 1963) have followed Van Beneden. We have discovered that Atlantic halibut is parasitised by 2 species of Entobdella , namely E. hippoglossi and a new species described below and referred to throughout our paper as “ E. hippoglossi type 2”. Baster’s illustrations (1759, fig. XI, a A) are so crude that it is impossible to determine which of the 2 species is represented. Consequently, although it is unclear why Van Beneden (1858) rejected Baster as the authority for E. hippoglossi , we agree with this decision. Müller’s description (1776) is clearly the first recognisable account of E. hippoglossi (see below) and Müller (1776) must be regarded as the authority for the species.

Müller’s fig. 4 (1776) (reproduced here as Fig. 33) shows clearly that there are few, relatively large, haptor papillae which are mostly arranged in radial rows. These are features of E. hippoglossi and not a new species described below. Furthermore, in Müller’s illustrations, there is no indication of a large vaginal opening. This feature could have been overlooked by Müller, since it is not always easy to resolve even with a modern microscope, but the details of the papillae strongly indicate that Müller’s brief description pertains to what we have called “ E. hippoglossi type 1”, that is E. hippoglossi sensu stricto, the type species of the genus.

Müller (1776) essentially comprises illustrations of external morphology. It was more than 80 years later when Van Beneden (1858) published a detailed and well illustrated account of the morphology and internal anatomy of parasites collected from H. hippoglossus . As with Müller’s work, the question must be asked whether Van Beneden was studying specimens of E. hippoglossi or the undescribed species to which we refer below. The sizes quoted by Van Beneden for his parasites (2.0 to 2.4 cm in total length) suggest that he may have been dealing not with E. hippoglossi (the total lengths of preserved adult “ E. hippoglossi type 1” in our collection range from 0.67 to 1.6 cm), but with the species that we have designated above as “ E. hippoglossi type 2” (the total lengths of preserved adult “ E. hippoglossi type 2” in our collection range from 1.39 to 2.22 cm). However, Van Beneden’s description of the distribution of the haptor papillae and his illustration of these (his Plate II, fig. 2; reproduced here as Fig. 34), together with the absence of any reference to a conspicuous vaginal opening surrounded by densely packed circular fibres, leaves no doubt that Van Beneden based his account on what we have called “ E. hippoglossi type 1”, that is on E. hippoglossi sensu stricto, the type species of the genus (but see further reference to the work of Van Beneden 1858 below).

A description as Epibdella hippoglossi was published by Cooper (1921) based on specimens collected in 1910 from H. hippoglossus from Le Have Island, Nova Scotia. A reference to “small tubercles” (= papillae) “radiating posteriorly” on the ventral surface of the haptor indicates that Cooper was describing E. hippoglossi ( Müller, 1776) Blainville, 1818 , not “ E. hippoglossi type 2” (see below).

The Greenland halibut, Reinhardtius hippoglossoides , and the Atlantic halibut, Hippoglossus hippoglossus occur in the North Atlantic Ocean. The identity of “ E. hippoglossi ” reported on R. hippoglossoides by Boje et al. 1997 is of great interest in view of our discovery that two species of Entobdella occur on H. hippoglossus . Our attempts to obtain specimens from R. hippoglossoides have not yet been successful (see Materials and methods).