Benedenia lutjani Whittington and Kearn, 1993

Whittington, I. D., Deveney, M. R. & Wyborn, S. J., 2001, A revision of Benedenia Diesing, 1858 including a redescription of B. sciaenae (van Beneden, 1856) Odhner, 1905 and recognition of Menziesia Gibson, 1976 (Monogenea: Capsalidae), Journal of Natural History 35 (5), pp. 663-777 : 713-720

Benedenia lutjani Whittington and Kearn, 1993

(®gures 9I±L, 10C, 12F)

Synonym. Tareenia lutjani ( Whittington and Kearn, 1993) Egorova, 1997 .

Material studied. QM: Nos GL13339±13343 (holotype and paratypes) (5 slides, 5 individuals) ex ®ns and body surface of Lutjanus carponotatus (Lutjanidae) from Heron Island, Queensland, Australia; QM: Nos G 217907±20 (vouchers) (14 slides, 14 individuals) ex branchiostegal membranes of L. carponotatu s ( Lutjanidae ) from Heron Island, Queensland, Australia; IDW: No. CAP334 (paratype) (1 slide, 1 individual) ex pectoral ®ns of L. carponotatus (Lutjanidae) from Heron Island, Queensland, Australia.

Comparative measurements of B. lutjani from Whittington and Kearn (1993) and from new material from the branchiostegal membranes are presented in table 5.

Observations. Whittington and Kearn (1993) carried out an extensive study of this species and examined live and preserved, mounted specimens as well as oncomiracidia and their work should be referred to for a detailed account of this species. Original measurements were based on 15 whole-mounts of specimens from the ®ns and body surfaces, but subsequently, fully grown adults of this parasite have been found to inhabit preferentially the branchiostegal membranes of their host (see Whittington, 1998 for a description of the branchiostegal membranes; Whittington and Ernst, in preparation).

Type-host and locality. Lutjanus carponotatu s ( Lutjanidae ), Heron Island, Great Barrier Reef, Queensland, Australia.

Published records. Whittington and Kearn (1993); Ernst and Whittington (1996); Whittington and Cribb (1999); Whittington and Ernst (in preparation).

Description. Whittington and Kearn (1993).

Published host record. Lutjanidae : Lutjanus carponotatu s.

Site . Found on all ®ns, predominantly the pelvic ®ns but also on body ¯anks and head ( Whittington and Kearn, 1993); adults inhabit preferentially the branchiostegal membranes (Whittington and Ernst, in preparation).

Distribution. Heron Island and Lizard Island, Great Barrier Reef, Queensland, Australia ( Whittington and Kearn, 1993).

Remarks. Whittington and Kearn (1993) compared B. lutjani with B. anticavaginata (see Byrnes, 1986) and T. (now Benedenia ) acanthopagri (see Hussey, 1986) because these are the only three species described with a vaginal pore anterior to the common genital pore. Benedenia lutjani can be distinguished easily from these Benedenia species by the following characters: the vaginal pore of B. acanthopagr i opens ventrally whereas that of B. lutjani and B. anticavaginata opens dorsally; B. lutjani has two small lobes associated with the common genital pore and a single lobe in the vicinity of the vaginal pore (®gure 10C) whereas B. acanthopagr i and B. anticavaginata each have a single lobe associated with the common genital pore (®gure 10A and B, respectively). Furthermore, B. acanthopagr i has considerably long anterior hamuli, almost twice the length of the posterior hamuli (®gure 9A, C, D) whereas in B. anticavaginata and B. lutjani , both pairs of hamuli are of similar length (®gure 9E, G, H, I, K, L). Benedenia anticavaginata is larger in terms of body and haptor size. The similarity between B. lutjani and B. anticavaginata suggest that they may be related closely.

Benedenia monticellii ( Parona and Perugia, 1895) Palombi, 1947 (®gures 12D, 25)

Synonyms. Epibdella monticellii Parona and Perugia, 1895 ; Epibdella (Phylline) monticelli ( Parona and Perugia, 1895) , Parona, 1896 ; Epibdella monticelli (Saint- Remy, 1898); Epibdella (Benedenia) monticellii (Monticelli, 1902) ; Benedenia (Parabenedenia) monticellii ( Johnston, 1929) ; Benedenia sp. of Paperna (1975).

Material studied. AC: No. 260 395 (2 slides, 1 with 15 specimens [all measured, see table 6], 1 with 48 specimens) ex Mugil sp. (probably M. cephalus L. according to Dr Angelo Colorni) from Gulf of Eilat, Israel [all these specimens now deposited as vouchers in HU; details below]; IP: (2 slides, 5 specimens) ex gills of, according to Professor Ilan Paperna, either Liza subviridis (Valenciennes in Cuvier and Valenciennes) or Valamugil seheli (ForsskaÊl) from the Gulf of Aqaba, Red Sea, Israel [all these specimens now deposited as vouchers in HU; details below]; IP: (13 slides, 14 specimens) (collected by Professeur Louis Euzet and Dr Alain Lambert) ex Mugil cephalus and Mugil capito (Cuvier) (5 Liza ramada Risso , see Thomson, 1990) ( Mugilidae ) from SeÁte, France [all these specimens now deposited as vouchers in various collections; details below]; NHML: Nos 1969.2.25.1 ±4 (1 slide, 4 specimens) (vouchers) ex gills of Oedalechilus labiosus (Valenciennes in Cuvier and Valenciennes) (5 Crenimugil labiosus Valenciennes , see Liu and Shen, 1991) ( Mugilidae ) from the Red Sea, Israel collected by Dr E. Trewavas.

Comparative measurements of some of the above material together with measurements from Parona and Perugia (1895) and Palombi (1947, 1949) are presented in table 6.

Vouchers. HU HUJ-MONO1.0,2.0 (2 slides, 63 specimens) ex Mugil sp. (probably M. cephalus according to AC), Gulf of Eilat, Red Sea, Israel; HU HUJ- MONO 3.0,4.0 (2 slides, 5 specimens) ex gills of Liza subviridis or Valamugil seheli (according to IP), Gulf of Aqaba, Red Sea, Israel; MNHN 832HF(Tk223±225) (3 slides, 3 specimens) ex M. cephalus from SeÁte, Medieterranean Coast of France; MNHN 832HF(Tk226) (1 slide, 2 specimens) ex M. capito (now L. ramada ) from SeÁte, Medieterranean Coast of France; NHML 2000.2.10.2 ±5 (4 slides, 4 specimens) ex M. cephalus from SeÁte, Medieterranean Coast of France; USNPC 089735-6 (5 slides, 5 specimens) ex M. cephalus from SeÁte, Medieterranean Coast of France.

Observations. We have been unable to obtain specimens of B. monticellii described by Parona and Perugia (1895) and those described by Palombi (1947). However, we have examined specimens thought to be B. monticellii provided by Dr A. Colorni and Professor I. Paperna from their private collections.

The original description by Parona and Perugia (1895) lacked su cient detail to be of use and contained little information about the reproductive system. Palombi (1947, 1949) referred to a common genital pore and vaginal pore forming a common genital atrium (see ®gure 4 in Palombi, 1947). When we compared material available to us with these accounts, a number of diOEerences were recognized that raised questions regarding the accuracy of these descriptions and / or the possibility that the specimens we procured are not the same as the`original’ B. monticellii of Parona and Perugia (1895) and Palombi (1947, 1949) but represent, perhaps, a diOEerent but closely related species. In particular, the`new’ specimens of B. monticellii have a common genital pore but the vaginal pore, although separate, is located close to the common genital pore (®gure 25A). Furthermore, a distinct muscular perimeter around the edge of the haptor, but inside the marginal valve, was observed in new material but this feature is not described in earlier accounts. Other distinguishing features we observed in the`new’ specimens of B. monticellii but which do equate well with the original descriptions of Parona and Perugia (1895) and Palombi (1947, 1949) include a haptor more transversely oval than round with distinct indentations on the posterior edge at the approximate positions of the posterior hamuli. However, haptor size relative to body size is smaller than described originally by Parona and Perugia (1895) (table 6).

Type-host and locality. Mugil auratus (Risso) (5 Liza aurata (Risso) Dor , see Thomson, 1990) ( Mugilidae ), Trieste, Italy.

Published records. Parona and Perugia (1895); Palombi (1947, 1949); Reichenbach-Klinke (1957); Paperna (1975) (as Benedenia sp. ); Paperna and Overstreet (1981); Paperna et al. (1984).

Descriptions. Parona and Perugia (1895); Palombi (1947, 1949).

Published host records. Gobiidae : Gobius paganellus (L.) (see Reichenbache- Klinke, 1957); Mugilidae :` Mugilidae of the genera Mugil and Crenimugil ’ (see Paperna, 1975); Crenimugil crenilabis (ForsskaÊl) (see Paperna et al., 1984); Liza carinata (Valenciennes ex Ehrenberg in Cuvier and Valenciennes) (see Paperna et al., 1984); L. ramada (see Paperna et al., 1984); L. subviridis (see Paperna et al., 1984); Mugil auratus (5 L. aurata, see Kottelat, 1997) (see Parona and Perugia, 1895; Palombi, 1947; Paperna and Overstreet, 1981); M. capito (see Palombi, 1947; Paperna and Overstreet, 1981); M. cephalus (see Paperna and Overstreet, 1981; Paperna et al., 1984); Valamugil seheli (see Paperna et al., 1984).

Site . Gills ( Parona and Perugia, 1895; Palombi, 1947); oral mucosa and body surface ( Paperna and Overstreet, 1981; Paperna et al., 1984);`dorsal ®n and integument surrounding the base’, oral mucosa, eyes ( Paperna et al., 1984).

Distribution. Trieste, Italy ( Parona and Perugia, 1895); Lago Fusaro, Italy ( Palombi, 1947); Gulf of Naples, Italy (Reichenbach-Klinke, 1957); SeÁte, France (see Euzet et al., 1993); Gulf of Eilat, El Bilaim Lagoon, Gulf of Suez, Israel ( Paperna, 1975); Eastern and Western Mediterranean Sea ( Paperna and Overstreet, 1981); Gulf of Eilat, El Bilaim Lagoon, A-Tor Bay, Gulf of Suez, Gulf of Aqabar, Israel ( Paperna et al., 1984).

Remarks. Confusion surrounds Benedenia monticellii! No type specimens were located to compare with the original description of B. monticellii by Parona and Perugia (1895) termed by Palombi (1947) as`imperfectly described’ or with the redescriptions by Palombi (1947, 1949). We studied a number of specimens from private collections identi®ed as B. monticellii in addition to four poor-quality specimens from the NHML identi®ed and removed from mullet in the museum’s ®sh collection and deposited by Dr E. Trewavas. DiOEerences noted between all specimens we have procured and previous descriptions of this species leave us unsure whether previous descriptions contained inaccuracies or whether the`new’ B. monticellii is actually a separate species, closely related to that described originally by Parona and Perugia (1895). Morphometrics of the diOEerent`groups’ of parasites are presented in table 6 and diOEerences between the available descriptions and specimens of B. monticellii are detailed below.

Parona and Perugia (1895) described this taxon from Mugil auratus (now Liza auratus ) oOE Trieste, Italy. It was distinguished from Benedenia (then Phylline ) species known then ( P. hippoglossi , P. sciaenae , P. hendor i, P. ishikawae and P. ovata ) by: presence of only two pairs of large haptoral sclerites instead of three pairs; diOEerences in body measurements; absence of papillae on the ventral surface of the haptor which was shown as circular with just a hint of posterior indentations (see drawing in Parona and Perugia, 1895: 85). Few useful details and no ®gure were provided about the reproductive system.

Palombi (1947) redescribed B. monticellii from the gills of Mugil capito (now Liza ramada ) from Lake Fusaro, Italy. The species was shown to have the following features: circular, apapillate haptor with inconspicuous indentations posteriorly (®gure 1 in Palombi, 1947); three pairs of large haptoral sclerites (thereby rectifying Parona and Perugia’s observation of two pairs of sclerites and therefore clarifying its inclusion in Benedenia ); median sclerites located on posterior half of haptor in his ®gure 1 but more posteriorly located in his ®gure 2; proximal ends of posterior hamuli were shown as having a`wish bone’ or Y-shape; common genital duct for penis and uterus and separate vaginal duct which unites distally to form common genital atrium; uterus joining penis canal half-way along its length.

Palombi (1949) appears to be a synthesis of Parona and Perugia (1895) and Palombi (1947) and provides no new information or ®gures.

Specimens of Paperna from Liza sp. (probably either L. subviridis or Valamugil seheli according to Professor Ilan Paperna) from the Red Sea, Israel. Unlike the two published descriptions (see above), these specimens have a vaginal pore separate from, but opening very close and just posterior to, the common genital pore (®gure 25A). The uterus joins the penis canal half-way along its length (®gure 25A). The penis has a broad shape which narrows dramatically distally to form a`teat’ shaped tip (®gure 25A). The accessory gland reservoir lies proximal to the penis and both penis and accessory gland reservoir lie inside a penis canal with a weakly muscular wall (®gure 25A). The body margin extends to the anterior edge of the anterior attachment organs (®gure 25A) giving the hooded appearance also depicted in ®gure 1B. The haptor is distinctively wider than long, with marked indentations at the positions of the posterior hamuli (®gure 25A). All of the large median sclerites are displaced posteriorly on the haptor and pigment cells are also visible throughout the haptor. The perimeter of the haptor proper (i.e. inside to the delicate marginal valve) is distinctly muscular (®gure 25A).

Specimens of Paperna from Mugil cephalus and M. capito (now Liza ramada ) from SeÁte, Mediterranean Coast of France. This material is characterized by: separate vaginal and common genital pores with the vaginal pore situated slightly posterior and dorsal to the common genital pore; the uterus joins the penis canal half-way along its length; the accessory gland reservoir is proximal to the penis, both structures lying inside the penis canal; the body margin extends to the anterior edge of the anterior attachment organs giving a`hooded’ appearance; the haptor is slightly oval, wider than long, with distinct indentations at the positions of the tips of the posterior hamuli; all of the large median sclerites are located posteriorly on the haptor; the anterior hamuli have distinctive`bulbous’ distal ends with subterminal spike and ®lamentous shaft; a distinct muscular rim is visible around the haptor proper. The shape of the penis, however, is variable: in some specimens, it appears broad with a narrow teat-shaped end but in others, the organ is narrow for its entire length. Further information concerning the relationship between the number of lobes of the marginal valve and the position of the 14 hooklets can also be added from these`new’ specimens of B. monticellii from Mugil cephalus and L. ramada as follows: one large lobe consisting of 12±13 fused lobes between the posterior hamuli; each hooklet of pair II is situated four lobes towards the mid-line from each posterior hamulus and there are four to ®ve fused lobes between these hooklets; a second large lobe consisting of seven fused lobes extends from the posterior hamuli to hooklet pair IV, with hooklet pair III being located three fused lobes from the beginning of this second large lobe; one large lobe comprising four small lobes between hooklets IV and V; one large lobe of seven to eight fused small lobes between hooklets V and VI; one large lobe of 9±10 small fused lobes between hooklets VI and VII; one large lobe of 12 fused, small lobes between hooklets VII and VIII; one large lobe consisting of 12±13 fused, small lobes between hooklets of pair VIII at the anterior margin of the haptor.

Specimens of Colorni from Mugil sp. (probably M. cephalus ; Dr Angelo Colorni, personal communication) from Israel. These specimens appear to be the same as those obtained by Paperna from the Mediterranean Sea (see above). Among them are some excellent specimens which display well details of the male and female reproductive systems. Some variation in sclerite shapes was observed and seems to be due to the orientation of specimens in the mounting medium.

Specimens from the Natural History Museum, London from Oedalichilus labiosus from the Red Sea, Israel. These specimens are smaller compared with the specimens of, for example, Paperna (table 6) but appear to have been very contracted when ®xed. This is consistent with the fact that these specimens were removed from ®xed mullet in the collection of the NHML (Dr David Gibson, personal communication). This material is of poor quality, few details are visible and the specimens are of limited use.

From our study, it appears that the specimens from Paperna and those collected by Colorni (see above) are similar morphologically and morphometrically (table 6) and seem likely to be the same species. There are, however, a number of diOEerences between these specimens and the descriptions provided by Parona and Perugia (1895) and Palombi (1947). One anomaly is the Y-shape description of the posterior hamuli by Palombi (1947, 1949) that we have not observed in our material. As table 6 shows, there are also substantial diOEerences in size between these`new’ specimens and the published descriptions of B. monticellii .

The specimens of B. monticellii obtained from Paperna and those collected by Colorni can be separated from other species of Benedenia by a combination of the following characters: vaginal pore slightly posterior and dorsal to the common genital pore; accessory gland reservoir relatively muscular; haptor oval-shaped, wider than long, with posteriorly located median sclerites; a distinctly muscular perimeter to haptor proper; prominent notches at the positions of the posterior hamuli (®gure 25A); anterior hamuli ®lamentous with distinctive`bulbous’ distal ends (®gure 25C); body margin extending to anterior edge of anterior attachment organs (®gure 25A).

Despite the advances we have made in piecing together a picture of what B. monticellii `may’ represent, further work is needed on the`new’ specimens of B. monticellii from the Red Sea and from France to determine whether it is the same as the benedeniine species described originally by Parona and Perugia (1895) or whether they represent a separate, but closely related, species. We consider it likely that the specimens from Paperna and Colorni are the`true’ Benedenia monticellii and that the original description by Parona and Perugia (1895) and other previous descriptions by Palombi (1947, 1949) contained errors. This conundrum can be resolved only by further collection of new specimens from the type-host ( Mugil auratus ) and type-locality (Trieste, Italy) for direct comparison with the original description of Parona and Perugia (1895), with Palombi’ s (1947, 1949) redescriptions and with the specimens identi®ed as B. monticellii by us from France and from the Red Sea, now lodged in various collections (see above).