Benedenia Diesing, 1858

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 : 667-680

Benedenia Diesing, 1858

Amended generic diagnosis. Capsalidae sensu Yamaguti (1963) . Benedeniinae (as amended above). Haptor with three pairs of large median sclerites (in anterior to posterior succession): accessory sclerites, anterior and posterior hamuli. Pair of haptor extrinsic muscles in body with long tendons entering haptor, passing through bi®d notch at proximal end of accessory sclerites, extending laterally, attaching to haptor tissue. Marginal valve scalloped. Ventral haptor surface apapillate. Anterior attachment organs usually disc-shaped (®gure 1B, C), sometimes elongate (®gure 1A), one on each side of anterior end (®gure 1); may be joined by membranous tissue providing`hooded’ appearance (®gure 1B) or appearing bipartite divided into anterior glandular (adhesive?) region and posterior more muscular (sucking?) region (®gure 1C). Vas deferens expands to form seminal vesicle anterior to testes. Male copulatory organ a penis occupying penis canal with weakly muscular wall; rarely equipped with terminal sclerite or conical papilla (e). Male accessory gland supplies single weakly muscular accessory gland reservoir proximal to penis, enclosed by proximal extension of wall of penis canal. Germarium with internal (fertilization?) chamber. Male and female genital apertures usually common, rarely separate (e.g. certainly for B. sciaenae ; possibly for B. pompatica and B. synagris ), opening near left side of body at level of pharynx. Vagina usually opening close to genital pore(s); rarely opening at mid-body between germarium and common genital pore (e.g. B. ovata ) or anterior to common genital pore (e.g. B. acanthopagr i, B. anticavaginata and B. lutjani ); distal part of vagina sometimes provided with musculature (e.g. sphincter in B. epinepheli ; ®gure 18). Eggs tetrahedral, usually with single, long appendage. Parasites of external surfaces, buccal cavity, branchial chamber and gills of marine teleosts.

Type species. B. sciaenae (van Beneden, 1856) Odhner, 1905 .

Other species. B. acanthopagr i ( Hussey, 1986) comb. nov.; B. anticavaginata Byrnes, 1986 ; B. bodiani Yamaguti, 1968 ; B. elongata ( Yamaguti, 1968) Egorova, 1997 ; B. epinepheli ( Yamaguti, 1937) Meserve, 1938 ; B. hawaiiensis Yamaguti, 1968 ; B. hendor i (von Linstow, 1889) Odhner, 1905; B. hoshinai Ogawa, 1984 ; B. innobilitata Burhnheim, Gomes and Varela, 1973 ; B. jaliscana Bravo-Hollis, 1952 ; B. lolo Yamaguti, 1968 ; B. lutjani Whittington and Kearn, 1993 ; B. monticellii ( Parona and Perugia, 1895) Johnston, 1929 ; B. ovata ( Goto, 1894) Johnston, 1929 ; B. pompatica Burhrnheim, Gomes and Varela, 1973 ; B. rohdei Whittington, Kearn and Beverley- Burton, 1994; B. scari Yamaguti, 1968 ; B. sekii ( Yamaguti, 1937) Meserve, 1938 ; B. seriolae ( Yamaguti, 1934) Meserve, 1938 ; B. synagris Yamaguti, 1953 .

Species inquirendae. Benedenia madai ( Ishii and Sawada, 1938) Price, 1939 ; B. pagrosomi ( Ishii and Sawada, 1938) Price, 1939 .

Remarks. Benedenia was proposed by Diesing (1858) for the species described as Epibdella sciaenae by van Beneden (1856). Benedenia has since had a complex history and for analyses, the following should be consulted: MacCallum (1927), Johnston (1929, 1931), Meserve (1938), Price (1939), Sproston (1946), Chauhan (1953), Lawler (1981), Byrnes (1986), Hussey (1986), Whittington and Kearn (1993) and Egorova (1997). The morphology of some species in this genus displays a high degree of variability ( Egorova, 1997) and several features which have been prominent in taxonomic discussions remain of unclear signi®cance. One area of contention regarding the taxonomy of Benedenia has been the problem of whether the`prostatic reservoir’ ( Yamaguti, 1963) (5 accessory gland reservoir) lies inside or outside the`cirrus pouch’ ( Yamaguti, 1963) (5 penis sac), a feature which Yamaguti (1963) used in his generic diagnosis and has been referred to by Byrnes (1986), Hussey (1986), Whittington and Kearn (1993) and Egorova (1997). This character was considered by Byrnes (1986) to be extremely di cult to determine in species in which the penis sac has a thin wall. Accordingly, Whittington and Kearn (1993) and Egorova (1997) excluded this character from their amended diagnoses of Benedenia and the Benedeniinae . After careful observation s of available specimens of Benedenia species , we have concluded that in all species of Benedenia , there is no structure that can be termed a`penis sac’. Instead, the penis occupies a penis canal with a weakly muscular wall and the accessory gland reservoir is proximal to the penis and is enclosed by a proximal extension of the wall of the penis canal (®gure 2A). This is distinct from the arrangement described in some benedeniines where the accessory gland reservoir lies at the proximal end of the penis, but both organs are enclosed clearly within a penis sac with muscular walls (e.g. Neobenedenia , see ®gure 2C). In describing the accessory gland reservoir as proximal to the penis, we conclude that the penis canal, at least in part, shares a wall with the accessory gland reservoir as shown in ®gure 2A because the two organs are contiguous. In most Benedenia species , the accessory gland reservoir itself has a mostly weakly muscular wall whereas the penis canal, while perhaps possessing some muscle ®brils, is not strongly muscular (®gure 2A). Indeed, in most Benedenia species examined, the penis canal consists merely of a membranous lining to the cavity in which the penis lies, but may be invested with a few poorly de®ned muscle ®bres. Exceptions to this are B. sciaenae and B. monticellii that possess a more muscular accessory gland reservoir.

In revising Benedenia , one of the most di cult tasks has been to`solidify’ the generic diagnosis and therefore the species composition because Benedenia contains many species de®ned by a range of morphological features which can display much variation. A genus, perhaps, can be considered to be a group of species with a morphological discontinuity between it and other related species. Although some benedeniine species may appear to form`species groups’ which have been interpreted by some as separate genera (e.g. Yamaguti, 1963; Gibson, 1976a, 1976b; Hussey, 1986; Egorova, 1997), we have decided to err on the side of caution and here retain most present Benedenia species in a single genus, Benedenia and, indeed, we synonymize Tareenia with Benedenia . A study of species belonging previously to Menziesia , however, has demonstrated, with the exception of `M. elongata ’, that these species are united by the form of their male copulatory organ and associated structures. Contrary to the ®ndings of Egorova (1997), we retain `M. elongata ’ as B. elongata but return B. noblei , B. merinthe and B. ovalis to Menziesia . We also recognize B. malaboni Velasquez, 1982 as Menziesia malaboni ( Velasquez, 1982) comb. nov. and B. sebastodis ( Yamaguti, 1934) Meserve, 1938 as M. sebastodis ( Yamaguti, 1934) comb. nov. A revised generic diagnosis for Menziesia is presented on p. 740, 744±745. These conclusions are supported by combinations of characters not used previously for all benedeniines such as the path of tendons in the haptor, the presence of the marginal valve (see Whittington and Kearn, 1993) in addition to the form of the male copulatory organ and associated structures. Observations of type material presented here include new features, often not examined or reported in original descriptions, including the arrangement of lobes on the marginal valve.

Another signi®cant problem has concerned the de®nition of the type species, B. sciaenae . When we commenced this study, few poor-quality voucher specimens of this species were available for examination and using these, we could not verify or refute several conīcting descriptions of B. sciaenae . We have examined in detail several specimens of this species from new material collected during this study and have nominated a series of voucher specimens. The taxonomy of Benedenia has been complicated by the seemingly divergent morphology of the` type species’ from its congeners. However, must a` type species’`de®ne’ a genus? Type species are often not`typical’ members of a genus and usually represent only the ®rst-described member of a genus. Although diOEerent from the majority of species ascribed to Benedenia , we do not consider currently that the diOEerences displayed by B. sciaenae from other species in the genus warrant separate generic status and here, we retain them as a single group.

Benedenia species show remarkable variation in size. For clarity and to demonstrate the size diOEerences, we have divided species into three size groups (®gure 3) and although some species may fall between our size groupings, we consider this arbitrary division useful in the preliminary steps of species identi®cation (see key to species of Benedenia on p. 739±740).

Benedenia sciaenae (van Beneden, 1856) Odhner, 1905 (®gures 4±8)

Synonyms. Epibdella n. sp. of van Beneden, 1852; Epibdella sciaenae van Beneden, 1856 ; Benedenia elegans Diesing, 1858 ; Tristomum sciaenae (van Beneden, 1856) Taschenberg, 1878 ; Phylline sciaenae (van Beneden, 1856) Sonsino, 1891 ; Epibdella (Phylline) sciaena (van Beneden, 1856) Parona, 1896 ; Epibdella (Benedenia) sciaenae (van Beneden, 1856) Monticelli, 1902 ; Benedenia (Benedenia) sciaenae (van Beneden, 1856) Johnston, 1929 .

Material studied. USNPC: No. 5270 (1 slide, 1 individual) from unspeci®ed site of unspeci®ed host from unspeci®ed locality (parasite identi®ed by Sonsino in November, 1892); USNPC: No. 5747 (1 unmounted specimen in alcohol) from unspeci®ed site of unspeci®ed host from unspeci®ed locality (parasite identi®ed by Sonsino, date unspeci®ed); USNPC: No. 7092 (1 slide, 1 individual) ex unspeci®ed site of Sciaena umbra (L.) ( Sciaenidae ) from unspeci®ed locality (parasite collected by Stiles in 1892); GCK: (2 slides, 2 individuals) ex skin of Sciaena antarctica (Castelnau) (5 Argyrosomus hololepidotus LaceÂpeÁde, see Trewavas, 1977) ( Sciaenidae ) from CoOEs Harbour, NSW, Australia; IDW: CAP 446-447 (2 slides, 2 individuals) ex unspeci®ed site of A. hololepidotus (Sciaenidae) from the Fisheries Research Institute ( FRI), Cronulla, Sydney, NSW, Australia; 73 slides, horizontal sections of 1 specimen; 78 slides, sagittal sections of 1 specimen; 50 slides, transverse sections of 1 specimen (specimens provided by Mr Dave Barker) ex body surfaces of A. hololepidotus (Sciaenidae) , FRI, Cronulla, Sydney, NSW, Australia; KR: (4 slides, 4 individuals) ex head of A. hololepidotus (Sciaenidae) from CoOEs Harbour, NSW, Australia [all of these specimens are deposited as vouchers in various collections (see below)]; MRD: 5 specimens (5 slides, 5 individuals) ex body surfaces of A. hololepidotus (Sciaenidae) , from Bate Bay, Cronulla, Sydney, NSW, Australia (specimens provided by Mr John Stewart); QM: Nos. G213151-5 9 (9 slides, 9 individuals) ex A. hololepidotus (Sciaenidae) from Victor Harbour, South Australia.

Vouchers. QM G 217921-2 (2 slides, 2 specimens); QM G 217923-4 (2 unmounted specimens in ethanol); NHML 2000.2.10 .1 (1 slide, 1 specimen on host scale); USNPC 089737.0 0 (1 slide, 1 specimen); all specimens ex head of A. hololepidotus (Sciaenidae) from CoOEs Harbour, NSW, Australia (collected by KR).

Redescription. Based on 15 whole-mounts of sexually mature specimens (13 from Australia, two from USNPC; table 1). Measurements made from 13 specimens from Australian hosts unless indicated otherwise (table 1). Table 1 presents a comparison of the morphometrics between Australian material, the two specimens from the USNPC and the few measurements presented in previous descriptions .

Total length including haptor 9100 ±19 500 (13 300); maximum breadth 3100±11 500 (6600) approximatel y at level of testes (®gure 4). Haptor almost circular, slightly wider at anterior end, 2200±6600 (4400)Ö3400±7400 (4800) (®gure 4). All large haptoral median sclerites positioned posteriorly (®gure 4). Accessory sclerites 480±1033 (725) long, blunt distal end,`winged’ for distal half, narrowing to uneven bi®d end proximally (®gures 4, 5A). Ridge of tissue extending from centre of haptor to accessory sclerites in most specimens (n 5 12) (®gure 4). Anterior hamuli 141±306 (246) long, pointed proximally with long, thin, ®ne recurved hook at distal end (®gures 4, 5B). Posterior hamuli 156±306 (222) long (n 5 20), with pointed proximal end; small hook distally (®gures 4, 5C). Signi®cant overlap of anterior and posterior hamuli (®gure 4). Hooklets (®gure 5D) 12±15 (12) long (n 5 6). Marginal valve scalloped with reasonably consistent number of lobes between hooklets on each side of haptor (from n 5 5 specimens): one small lobe between hooklets of pair II on posterior border of haptor; two small lobes between hooklets II and III; one small lobe between hooklets III and IV and between hooklets IV and V; one larger lobe comprising several fused, smaller lobes between hooklets V and VI and between hooklets VI and VII; one large lobe comprising several fused, smaller lobes between hooklets VII and VIII and between hooklets of pair VIII on anterior border of haptor (®gure 4) .

Anterior attachment organs sub-circular (®gures 4, 7A) 430±2372 (1370)Ö 758±2499 (1627), appearing more muscular than glandular. Anterior extremity of body margin extends between anterior attachment organs to their anteriormost edges (®gure 4). Lens remnants associated with eyes in seven specimens. Pharynx 727±1785 (1189)Ö636±1594 (1085) with intrinsic gland cells. Gut consists of ®ne dendritic network, not conūent posteriorly.

Glands of Goto not visible in posterior angle between testes in any specimens studied, but similar organs observed in anterior angle between testes in four specimens (®gure 4). Vas deferens swells to form distinct seminal vesicle between testes and germarium (®gure 4); convoluted vas deferens passes dorsal to ootype, then travels dorsally to base of penis before descending to enter proximal part of penis ventrally (®gures 4, 6A). Vas deferens and accessory gland reservoir duct unite near tip of penis (observed clearly in one specimen only; ®gure 6B). Penis narrowing, elongate, tapered (®gure 6A). Accessory gland reservoir relatively thick-walled, with some muscles (®gure 6A). One bundle of ®ne accessory gland ducts enters proximal end of accessory gland reservoir (observed in one specimen only). Male genital pore opens marginally, anteromost of three genital pores (®gures 4, 6A, 7A, B).

Ootype sometimes containing egg-shell material (®gure 6A). Uterus long, also sometimes containing egg-shell material, dorsal and slightly posterior to male genital canal in four specimens; lies dorsal to and separate from penis canal, terminates via distinct, separate uterine pore slightly dorsoposterior to male pore (®gures 4, 6A, 7B). Proximal end of vagina widens to form chamber (®gure 4) often containing spermatozoa; communicates via narrow duct with vitelline reservoir. Terminal (distal) region of vagina a narrow tube. Vaginal pore on dorsal surface close to lateral margin (®gure 7C), posterior, slightly dorsal to uterine pore (®gures 4, 6A, 7C, D). Eggs tetrahedral, sides 133±184 (157) long (n 5 5 eggs measured in utero); slender appendage from one of three non-opercular poles visible but not measured.

Pigmentation on dorsal side of body and haptor as shown in ®gure 8.

Type-host and locality. Sciaena aquila (Cuvier) (5 Argyrosomus regius Asso , see Trewavas, 1973) ( Sciaenidae ), Slykens, at the mouth of the port of Ostende, Belgium.

Published records. van Beneden (1852, 1856, 1858); Sonsino (1891); Monticelli (1892); Stiles and Hassall (1894); Goto (1894, 1899); Froissant (1930); Palombi (1949); Kuznetzova (1975); Euzet et al. (1993); Whittington (1996).

Descriptions. van Beneden (1852, 1856, 1858); Goto (1899); Palombi (1949); present study.

Published host records. Myliobatididae : Myliobatis aquila L. (see Kuznetzova, 1975). Sciaenidae : Sciaena aquila (5 Argyrosomus regius ) (see van Beneden, 1852, 1856, 1858); Umbrina cirrhosa (sic, probably U. cirrosa L.) (see Sonsino, 1891); Sciaena umbra (L.) (see Sonsino, 1891; Monticelli, 1892); Argyrosomus regius (see Euzet et al., 1993); Argyrosomus hololepidotu s (see Whittington, 1996; present study).

Site . Skin.

Distribution. Ostende, Belgium (van Beneden, 1856); Viareggio, Pisa, Italy ( Sonsino, 1891);`French Waters’ ( Froissant, 1930); Patagonian Shelf ( Kuznetzova, 1975); Mediterranean Sea, France ( Euzet et al., 1993); CoOEs Harbour and Cronulla, NSW and South Australia, Australia (Whittington, 1996).

Remarks. No type material of B. sciaenae was designated by van Beneden and this made our study a di cult task. Hussey (1986) also attempted to ®nd type specimens but failed. We did trace three specimens identi®ed as B. sciaenae lodged in the USNPC and two of these were included in our investigation (table 1). Our redescription has been assisted greatly by the discovery of new material from South Australia and New South Wales, Australia (Whittington, 1996). Although our new material is from neither the type-host nor the type-locality, from previous descriptions and from specimens available from the USNPC, we are con®dent that the Australian material is B. sciaenae (see Whittington, 1996 and table 1). The new material has allowed a redescription of B. sciaenae and has clari®ed a few points of confusion regarding its anatomy. We regard it likely that the record of B. sciaenae from the ray Myliobatis aquila (Myliobatididae) by Kuznetzova (1975) was a misidenti®cation and that this discovery may be a species of Benedeniella Johnston, 1929 .

Benedenia sciaenae was ®rst discovered by van Beneden (1852) on the surfaces of the`European lean ®sh’, Sciaena aquila (now Argyrosomus regius ) at Ostende, Belgium, but a description and ®gure were not published by van Beneden until 1856. Separate pores for the male copulatory organ and the uterus are depicted by van

± Indicates that no measurements were presented for these characters.

* Goto (1899) did not state speci®cally that only one specimen was used, but the specimen was referred to in the singular throughout his account.

²The 13 Australian specimens measured are: KR: 4 specimens now deposited as vouchers in NHML 2000.2.10. 1; QM: Nos G 217921±2; USNPC 089737 .00; plus QM: Nos G 213151±59 (9 specimens) .

‡The two US specimens measured are: USNPC: Nos 5270 and 7092.

Beneden (1856), but these features are not mentioned in the text. van Beneden (1858) gave a further detailed account of B. sciaenae in which separate male and female pores are again described. Each of these accounts by van Beneden (1852, 1856, 1858) is excellent and incorporates detailed observations made on live worms including a description of egg-laying. Since van Beneden clearly watched these events closely, we suggest that his description of separate male and female pores that open close to each other is correct. Our study of new but preserved material from Australia has con®rmed his opinion although in many specimens it is often exceedingly di cult to trace accurately the positions and routes of the separate ducts and the exact location of their openings. Light microscopy and SEM (®gure 7) has demonstrated that van Beneden’s opinion on the presence and route of separate male and female ducts and pores and of the route of the vagina and location of the vaginal pore was correct. The arrangement of the vas deferens and of the duct exiting the accessory gland reservoir and travelling inside the penis is also very di cult to observe in the specimens available. These ducts are visible only distal to the narrowing in the penis in ®ve specimens and in only one specimen can the ducts be observed to unite near the tip of the penis (®gure 6B).

Redescriptions given by Goto (1899) and Palombi (1949) diOEer from those by van Beneden and us. Goto (1899) studied a single specimen belonging to Stiles which was originally supplied to him by Sonsino (it is possible that the specimen he studied was either USNPC No. 5270 or 7092) and concluded that the uterus was`very short’ because it joined the`penis sac’ at its base rather than running parallel with, and separate from, the penis canal containing the penis. Similarly, Palombi (1949) redescribed B. sciaenae and followed Goto’s scheme. From our investigation of deposited museum material and of new material, we conclude that B. sciaenae does indeed have separate pores for the male copulatory organ and for the uterus, the male pore opening just anterior to the uterine pore (®gures 4, 6A, 7A, B). Since these pores are so close together and since the vagina opens slightly posterior to the uterus, we can see why the arrangement may be misinterpreted, even after careful observation, because all three ducts can appear to open into a common genital pore or atrium as stated by Goto (1899), Palombi (1949) and Hussey (1986).

van Beneden (1856, 1858) reported dark ruby pigment located dorsally and scattered throughout the body, haptor and anterior attachment organs. This coloration obviously camouāged the parasites against the surface of the ®sh because van Beneden (1856: 504) noted that it required much concentration to ®nd this parasite, and stated that many naturalists may have held specimens of the ®sh before their eyes without recognizing the worms (paraphrased translation from French). Palombi (1949) also referred to red markings dorsally in B. sciaenae . Most of the preserved specimens studied by us from the USNPC and those collected in Australia also had dark brown or black pigment throughout the body and haptor (see ®gure 8 in the present study and ®gure 3 in Whittington, 1996). Whittington (1996) and Deveney and Whittington (in press) have described pigmentation in other benedeniines and also examined the somatic pigment of B. sciaenae .

van Beneden (1858) made a close comparison between Epibdella (now Entobdella ) hippoglossi (MuÈller, 1776) Johnston, 1856 and Epibdella (now Benedenia ) sciaenae and commented that papillae which covered the ventral surface of the haptor of E. hippoglossi were not as common on the ventral surface of the haptor of B. sciaenae . Papillae have been noted on the ventral haptor surfaces of E. hippoglossi and E. soleae by Lyons (1973) but not in other species of the genus ( Whittington and Barton, 1990). Papillae of this kind were not observed in the present study of B. sciaenae and we consider that haptoral papillae are absent from all Benedenia .

In our material of B. sciaenae , we could not identify clearly a chamber inside the germarium containing ripe oocytes and sperm, but van Beneden (1858) described such an organ in B. sciaenae from his observations on live worms.

We have termed the male copulatory organ of B. sciaenae a penis because, from whole-mounts and sections, it appears to be a protrusible muscular organ rather than an eversible structure. Among Benedenia species , the penis of B. sciaenae is unusual because it tapers distally. In no whole-mount studied was the penis observed to protrude from the male pore. It is interesting to note, therefore, that van Beneden (1858, p. 29) observed that the male duct terminated in a mobile papilla which unrolled like the ®nger of a glove (paraphrased translation from French), a description that would seem to describe the eversion of a cirrus. There is clearly much to resolve about the male copulatory organ of B. sciaenae and, indeed, of all species of Benedenia , but until observations or reports to the contrary, we consider the male organ in this species to be a penis as it appears to be in all species of the genus.

We have determined that the accessory gland reservoir of B. sciaenae (which is more muscular than in most Benedenia species ) lies proximal to the penis and both structures occupy a penis canal which has a weakly muscular wall (®gure 6A). There is no structure akin to the more muscular penis sac described for some benedeniines such as Neobenedenia (®gure 2C). These anatomical features (accessory gland reservoir, penis and penis canal) are often poorly represented in literature on benedeniines and especially for Benedenia .

van Beneden (1852, 1856, 1858), Goto (1899) and Palombi (1949) did not mention the presence of glands of Goto in B. sciaenae . We have not observed these organs in their`usual’ site in the posterior angle between the testes. However, in a few of the Australian specimens, two organs similar to glands of Goto were observed in the anterior angle between the testes (®gure 4). Structures thought to be glands of Goto have been reported in this region in Allobenedenia ishikawae ( Goto, 1894) Yamaguti, 1963 and possibly in Trimusculotrema uarnaki Whittington and Barton, 1990 (see the`conspicuous cells’ of Whittington and Barton, 1990) and this deserves further study.

Benedenia sciaenae can be distinguished clearly from all species in the genus by a combination of: its large size; possession of separate but closely apposed male and female pores; long, tapering penis; glands of Goto(?) lying anterior to the testes; and the posterior position of the large accessory sclerites possessing distinctive surrounding tissue in the haptor.