Benedenia acanthopagr

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 : 680-685

Benedenia acanthopagr i ( Hussey, 1986) comb. nov.

(®gures 9A±D, 10A, 12E)

Synonym. Tareenia acanthopagr i Hussey, 1986 (new synonym).

Material studied. NHML: No. 1984.9.13 .1 (holotype and paratype) (1 slide, 2 specimens: holotype labelled 1984.9.13.1; another specimen on same slide labelled paratype); NHML: No. 1984.9.13.2-11 1 (paratypes) (5 slides including 2 slides of sections, 3 slides each with 1 whole-mount) ex skin of Acanthopagrus latus (Houttuyn) (Sparidae) from ®sh in culture tanks at Al-Raas, Kuwait.

Observations. The original description matches the type specimens of Tareenia acanthopagri and Hussey (1986) should be consulted for a detailed account. We wish to point out a few important details about the anatomy of this worm. The marginal valve has a characteristic arrangement of lobes which was represented faithfully by Hussey (1986; his ®gure 1) but not described. From our study of type material, the arrangement is shown in ®gure 9A and can be described as: one lobe between hooklets of pair II on the posterior border of haptor; one lobe between each hooklet of pair II and position of hamuli tips; one lobe between position of hamuli tips and each of hooklet pair III; one lobe between hooklets III and IV, between IV and V, and between V and VI; up to nine small lobes (appearing fused) between hooklets VI and VII; approximately 10 small lobes (appearing fused) between hooklets VII and VIII; numbers of lobes between hooklets of pair VIII di cult to determine (details obscured by body proper) but Hussey (1986; ®gure 1) shows nine small (fused) lobes, which are visible in a scanning electron micrograph in his ®gure 7.

Other features of the haptor deserve comment. It has an unusual shape described by Hussey as resembling an`inverted tulip ¯ower’. The anterior hamuli are extremely long and span almost half the total length of the haptor (®gure 9A). The anterior hamuli just overlap the proximal ends of the accessory sclerites and, in some specimens, overlap totally the posterior hamuli (®gure 9A) whereas in other specimens, the posterior hamuli extend beyond the distal tips of the anterior hamuli.

Hussey (1986) erected Tareenia on the basis of two features: the vaginal pore opening anterior and ventral to the common genital pore and the presence of a ventral ¯ap which overlies the common genital pore (®gure 10A). The ventral ¯ap is clearly visible in type material but the anterior route of the vagina and its pore is very di cult to see in the types. Much of the rest of this species appears to be typically Benedenia -like. Hussey (1986) commented that he could not determine, even in sectioned material, whether the accessory gland reservoir was located inside the penis sac. Our investigation has shown that the wall of the penis canal is weakly muscular as is the accessory gland reservoir ( Hussey, 1986; ®gure 8) which lies proximal to the penis and is enclosed by a proximal extension of the wall of the penis canal. Hussey (1986) described, and we con®rm, that glands of Goto are present in the posterior angle between the testes.

Type-host and locality. Acanthopagrus latus (Sparidae) , in culture tanks, Al-Raas, Kuwait.

Published record and description. Hussey (1986).

Published host record. Sparidae : Acanthopagrus latus .

Site . Skin.

Distribution. From ®sh held in culture at Al-Raas, Kuwait.

Remarks. With the evidence available to him at the time, we consider Hussey’s judgement to establish a new genus, Tareenia , based on two unique characters, (1) vagina opening anterior and ventral to common genital pore and (2) ventral ¯ap near the submarginal common genital pore (®gure 10A), to be reasonable. However the progressive revision of some benedeniine genera, the clari®cation of some generic characters and recent descriptions of two species also with an anterior vagina, but placed in Benedenia , calls for a reappraisal of Tareenia .

Tareenia acanthopagr i from the skin of Acanthopagrus latus (Sparidae) from Kuwait was the ®rst benedeniine described to possess a vagina opening anterior to the common genital pore (®gures 10A, 12E). Subsequently, however, two benedeniine species with an`anterior vagina’ have been described and placed in Benedenia . Byrnes (1986) described B. anticavaginata from`under pectoral ®ns’ of Acanthopagrus australis (Owen) and A. berda (ForsskaÊl) (Sparidae) in Australia, with a vagina opening anterior to the common genital pore on the dorsal surface (®gure 10B). Whittington and Kearn (1993) reported B. lutjani with a vagina also opening anterior to the common genital pore on the dorsal surface of the parasite (®gures 10C, 12F) from all ®ns (predominantly the pelvics) but also from the body ¯anks and head of Lutjanus carponotatus (Richardson) (Lutjanidae) in Australia. At least one other Benedenia species , as yet undescribed, with a vagina opening anterior and dorsal to the common genital pore, is known to occur on the gills of Diagramma labiosum (Macleay) (Haemulidae) in Australia (Whittington and Deveney, previously unpublished observation). Recently, Egorova (1997) placed B. lutjani and B. anticavaginat a in Tareenia , but she did not resolve fully the similarities and diOEerences between these species. Hussey (1986) agreed his new species ®tted the concept of Benedenia as interpreted by several authors but compared it directly with the type species, B. sciaenae . Although not stating so, Hussey appeared to base his comparisons of T. acanthopagr i on redescriptions of B. sciaenae by Goto (1899) and Palombi (1949) and considered, therefore, that B. sciaenae possessed a common genital pore which united with the vaginal pore to form a common genital atrium. Hussey commented that B. sciaenae diOEered, therefore, from most other species later allocated to Benedenia and suggested the desirability of restricting Benedenia to species with this character. We demonstrated above, however, that B. sciaenae is as originally described by van Beneden (1856, 1858), possesses separate male, female and vaginal pores and have revised the generic diagnosis to accommodate this. It was further argued by Hussey (1986) that the anterior position of the vaginal pore in T. acanthopagr i may be an important taxonomic character reēcting the reproductive behaviour and method of sperm exchange in this species. Egorova (1997) based her opinion of the generic composition of Tareenia largely on the anterior position of the vagina. We argue, however, that an anterior shift in the position of the vaginal opening seems unlikely to have large repercussions for the way the parasites approach each other during mating. Figure 11 shows diagrammatically that there is likely to be little diOEerence in the way species with a vagina located anterior to the common genital pore mate (®gure 11B) in comparison with species possessing a vagina posterior to the common genital pore (®gure 11A). Furthermore, Kearn and Whittington (1992) demonstrated that diOEerent species of Benedenia can cross-inseminate in at least two diOEerent ways: by spermatophore s or by intromission without spermatophores. Thus, there is a need to determine more about the speci®c method(s) of copulation in species with an anteriorly located vaginal pore before schemes proposing diOEerent reproductive behaviours and reproductive isolation are propounde d further.

On present evidence, we consider that the position of the vaginal pore is a speci®c variable that has probably evolved more than once in this group of monogeneans. Other diOEerences in the position of the vagina occur elsewhere in species of Benedenia (following our conception of the genus) and ®gure 12 shows the continuum of variation we have observed. The vagina of B. sciaenae opens close, but just posterior, to the separate male and female pores (®gures 4, 6A) and a similar position has been noted of the vagina relative to the common genital pore in B. monticellii (®gure 12D) whereas in B. ovata Goto, 1894 , the vagina opens far more medioposteriorly (®gure 12A); there are other, intermediate conditions for the position of the vaginal pore depicted in ®gure 12B, C. Presently, we consider the best course of action is to include all species with diOEerent vaginal pore positions but otherwise of similar morphology in Benedenia pending further investigations. It is possible that the continuum of speci®c variation in the position of the vagina may become more evident as more species are described, thus making the diOEerentiation between species with an`anterior’,`median’ or`posterior’ vagina redundant. Furthermore, within species described with an`anterior’ vagina, there is variation in the location of the vaginal pore: in B. acanthopagr i, the pore is ventral whereas in B. anticavaginata and B. lutjani , the pore is dorsal. Thus our decision is that Tareenia Hussey, 1986 be synonymized with Benedenia and the three species, T. acanthopagr i, T. anticavaginata and T. lutjani of Egorova (1997) become Benedenia acanthopagr i comb. nov., B. anticavaginata and B. lutjani , respectively. If future studies should show extra and signi®cant uniting characters between these species other than the anterior position of the vaginal pore, their generic status should be reappraised further.

The ventral ¯ap close to the ventral common genital pore was another important character in Hussey’s decision to erect Tareenia . The report of prominent lobes associated with the common genital pore in B. lutjani by Whittington and Kearn (1993) (®gure 10C) and the discovery during the present study of a lobe associated with the common genital pore of B. anticavaginata (®gure 10B and p. 685), may appear at ®rst, to support the validity of Tareenia , but the presence of lobes and ¯aps has been noted in other species of Benedenia which do not possess an`anterior vagina’, such as B. epinepheli as redescribed by Ogawa et al. (1995) and B. hawaiiensis as reappraised in this study. The number, shape and position of these lobes and ¯aps diOEer between species, their role is unknown, and it remains to be determined whether the diOEerent protuberances have similar functions.

Benedenia acanthopagr i can be distinguished from other Benedenia species that possess an`anterior vagina’ by: the position of its vaginal pore which is ventral; the presence of a ventral ¯ap from the body which covers the common genital pore (®gure 10A); the unusual shape of the haptor (®gure 9A); the presence of very long, slender and straight anterior hamuli which span almost half the total length of the haptor, which overlap the accessory sclerites proximally, and which entirely or almost entirely overlap the posterior hamuli (®gure 9A).

Figures

FIG. 11. Orientation of co-copulants during sperm exchange as observed for (A) Entobdella soleae (after Kearn, 1970); scale bar 5 1 mm. (B) Likely orientation of co-copulants for a species of Benedenia with a vaginal pore anterior to the common genital pore (based on B. lutjani); scale bar 5 500 Mm. Note that the probable orientation by which benedeniines with a vaginal pore opening anterior to the common genital pore may align themselves is likely to be similar to that of species which possess a vaginal pore that opens posterior to the common genital pore, such as E. soleae.