Benedenia hawaiiensis Yamaguti, 1968

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 : 698-704

Benedenia hawaiiensis Yamaguti, 1968

(®gures 16C, 19G±I, 20)

Material studied. USNPC: No. 63587 (holotype and paratypes) (1 slide, 14 specimens; holotype marked) ex gills and ®ns of Priacanthus cruentatus (LaceÂpeÁde) ( Priacanthidae ), Hawaii; MPM: No. 15393 (paratypes) (1 slide, 6 specimens) ex Holocentrus scythrops ( Jordan and Evermann) (5 Neoniphon aurolineatus LieÂnard , see Randall and Heemstra, 1985) ( Holocentridae ), Hawaii; MPM: No. 15394 (paratypes) (2 slides, 1 with 1 specimen, 1 with 6 specimens) ex Parupeneus pleurostigma (Bennett) (Mullidae) , Hawaii; MPM: No. 15395 (paratypes) (1 slide, 1 specimen) ex P. bifasciatus (LaceÂpeÁde) ( Mullidae ), Hawaii; MPM: No. 15396 (paratypes) (2 slides, 1 with 16 specimens, 1 slide with 17 specimens) ex P. porphyreus (Bennett) (Mullidae) , Hawaii; MPM: No. 15397 (paratypes) (2 slides, 1 with 13 specimens, 1 with 1 specimen) ex Dascyllus albisella (Gill) (Pomacentridae) , Hawaii; MPM: No. 15398 (paratypes) (1 slide, 1 specimen) ex Acanthurus nigrofuscus (ForsskaÊ l) ( Acanthuridae ), Hawaii. Yamaguti (1968) noted that B. hawaiiensis was found on the gills and body surface of the type host, but did not specify a site for other host species.

The 58 specimens, for which comparative measurements are presented in tables 2 and 3, are itemized fully in table 3 for each host species. Note that one specimen from H. scythrops (5 N. aureolineatus), one specimen from Priacanthus cruentatus and the single specimen from Parupeneus bifasciatus could not be measured because the material was either immature or of poor quality.

Observations. Yamaguti (1968) based his description on 52 whole-mounts of which 13 were from the type-host. He listed 24 ®sh species in 10 families from four orders as hosts to B. hawaiiensis . In lists supplied to us by the Meguro Parasitological Museum, of 24 diOEerent`lots’ of specimens, only the slides we examined were designated as types. We examined a total of 76 specimens (58 were measured; table 3)

± Indicates that no measurements were made due to folding of the specimen.

from seven diOEerent host ®sh species. While some diOEerences in size between the parasite specimens from diOEerent hosts exist, the material is mostly of similar morphology. Morphological diOEerences noted between specimens from diOEerent hosts include: narrow versus broad bodied parasites; diOEerences in the sizes of the anterior attachment organs and haptor relative to the body; diOEerences in the shapes and sizes of the testes; the conspicuous presence or apparent absence of glands of Goto; presence or absence of a lobe on the body margin close to the common genital pore; diOEerences in the conspicuousness of the vagina; presence or absence of`wavy’ muscle near the edge of the haptor. Some specimens from the same host species and on the same slides appear to have diOEerent body and sclerite shapes and show some diOEerences in internal anatomy.

Benedenia hawaiiensis was well-described by Yamaguti (1968) but the following supplementary information is given. Yamaguti (1968) described the accessory sclerites as alate but we have determined that the alae are raised ventral haptoral tissues through which the accessory sclerites protrude. The path of tendons in the haptor is shown in ®gure 16C. The proximal ends of the anterior hamuli overlap with the proximal ends of the accessory sclerites and the distal portion of the anterior hamuli overlap with the posterior hamuli for two-thirds of their length. Yamaguti recorded only 12 hooklets but we counted 14 (®gure 16C). In most specimens, the marginal valve is clearly indented at each hooklet and also at the position where the posterior hamuli meet the haptor edge. The marginal valve is conspicuous and has one lobe between each of the hooklets around the circumference of the haptor with the anterior lobes being larger and wider; there was no evidence that each larger, anterior lobe was composed of several smaller lobes (®gure 16C). In some specimens, conspicuous wavy muscles were evident near the haptor edge but this was not consistent, unlike B. bodiani and B. scari , where this feature was observed consistently.

The penis was reasonably well-depicted by Yamaguti (1968) but, as for B. scari , he appears to have misinterpreted the structure of the penis sac and penis. Our investigation shows that the penis is muscular, well-equipped with circular and longitudinal muscle ®bres and lies in a cavity or canal with poorly developed muscle in its walls (®gure 20). The most prominent and notable features of the penis of B. hawaiiensis are that it tapers to form a narrow distal tip in most specimens examined (®gure 20) but in some, the penis was observed to have a broader tip. Yamaguti described the`ejaculatory duct’ (5 vas deferens) and the`prostatic duct’ (5 duct of the accessory gland reservoir) as joining at the base of the`cirrus’ (5 penis) but this appears to reēct his view that the`cirrus’ was the tapered distal portion of the entire male copulatory organ. We have determined that the duct from the accessory gland reservoir and the vas deferens join at or near the penis tip. The glands of Goto in B. hawaiiensis are not a good diagnostic character because, as indicated above, they were easily observed in some specimens but not in others.

We could not see a fertilization chamber inside the germarium. In some material, a lobe was observed near the common genital pore (for instance, in specimens from Dascyllus albisella and Parupeneus porphyreus ) but not in other material. In most specimens, the vagina appeared to be a narrow duct with a funnel-shaped termination (®gure 20). However in all specimens examined from D. albisella , the vagina appeared wider and more prominent along its entire length due to muscular walls.

Type host and locality. Priacanthus cruentatus (Priacanthidae) , Hawaii.

Published record and description. Yamaguti (1968).

Published host records. Aulopiformes : Synodontidae : Synodus dermatogenys (Fowler) ; Beryciformes : Holocentridae : Holocentrus scythrops ; H. spinifer (probably Sargocentro n spiniferum ForsskaÊ l); Perciformes : Acanthuridae : Acanthurus dussumi - eri (Valenciennes in Cuvier and Valenciennes); A. nigrofuscus ; Naso hexacanthus (Bleeker) ; Chaetodontidae : Chaetodon miliaris (Quoy and Gaimard) ; Mullidae : Mulloidichthys samoensis (GuÈnther) (5 Mulloidicthys X avolineatus LaceÂpeÁde, see Randall et al., 1998); Parupeneus bifasciatus (LaceÂpeÁde); P. chryserydris (probably P. chryserydros LaceÂpeÁde, now P. cyclostomus LaceÂpeÁde, see Randall et al., 1998); P. multifasciatus (Quoy and Gaimard) ; P. pleurostigma ; P. porphyreus (probably Pseudupeneus porphyreus Jenkins ); Pomacentridae : Abudefduf abdominalis Quoy and Gaimard ; Chromis ovalis Steindachner ; Dascyllus albisella ; Priacanthidae : Priacanthus cruentatus ; Scaridae : Scarus sordidus (ForsskaÊl) (5 Chlorurus sordidus Swainson , see Bellwood, 1991); Tetraodontiformes : Monacanthidae : Alutera scripta (probably A. scriptus Osbeck ); Amanses carolae ( Jordan and MacGregor); A. pardalis (Gray) (5 Cantherhines pardalis RuÈppel , see Masuda et al., 1988); A. sandwichiensis (Quoy and Gaimard) ; Pervagor spilosoma (Lay and Bennett) ; Balistidae : Xanthichthys ringens (L.).

Sites. Gills and body surface (sites recorded for type host species, Priacanthus cruentatus , only).

Distribution. Hawaii.

Remarks. Benedenia hawaiiensis is a problematic species because many specimens are available for study from many diOEerent host species. The species has not been recorded since Yamaguti’s (1968) work in Hawaii. Our observations indicate that while most specimens can be recognized as belonging to the same species, there is some concern about the species identity of some specimens. Most notable is material from D. albisella which diOEers from most other material by the muscular appearance of the vagina and the presence of a lobe near the common genital pore. It is worth bearing in mind that Yamaguti collected parasite material from 17 other host species, specimens of which we were unable to examine. On the basis of material at our disposal, we have elected to err on the side of caution and consider that all his specimens belong to a single species. Yamaguti (1968) collected much material from ®shes purchased at Honolulu ®sh market and sometimes obtained hosts from the Waikiki Aquarium of the University of Hawaii. It is unfortunate that Yamaguti did not state which material was from which source because it seems likely that ®sh species bought at markets may have been stored for some time with diOEerent ®sh species allowing the possibility for parasites to transfer or`fall’ from one host species to another. Benedenia hawaiiensis appears to have low host-speci®city like Neobenedenia melleni (see Whittington and Horton, 1996) and B. epinepheli (see p. 694). Future collections from Hawaiian ®shes directly from the wild may determine whether B. hawaiiensis does comprise a single species and whether or not it can parasitize as many hosts as Yamaguti reported.

Yamaguti (1968) stated that B. hawaiiensis was most similar to B. epinepheli . We concur that these two species are close relatives. Figure 16B, C shows the similar haptor morphology for these two species and ®gure 19 illustrates the shapes of their haptoral sclerites, although the relative sizes of the sclerites of B. epinepheli are a little smaller (see also ®gure 16B, C and table 2). Another similarity is the broad, muscular penis (compare ®gures 18 and 20). The two species can be distinguished on present evidence, however, by the characteristic, narrow, tapered tip of the penis in B. hawaiiensis compared with the broader penis tip in B. epinepheli (cf. ®gures 20 and 18, respectively). Benedenia epinepheli possesses an anteriorly directed lobe near the common genital pore which is not present in most material of B. hawaiiensis . Furthermore, B. epinepheli has a prominent lobe associated with the vagina whereas no such lobe was observed in any specimens of B. hawaiiensis . It is interesting that B. hawaiiensis and B. epinepheli are similar morphologically and these two species also display the lowest host-speci®city reported among species of Benedenia .

Benedenia hendor i (von Linstow, 1889) Odhner, 1905 (®gure 21)

Synonyms. Phylline hendor i von Linstow, 1889; Epibdella hendor i (von Linstow, 1889) Braun, 1890; Epibdella hendor i (von Linstow, 1889) Monticelli, 1891; Phylline endor W i von Linstow of Parona and Perugia, 1895 (see Lawler, 1981); Epibdella (Phylline) hendor i (von Linstow, 1889) Heath, 1902; Epibdella (Benedenia) hendor i (von Linstow, 1889) Monticelli, 1902; Benedenia hendor i (von Linstow, 1889) Stiles and Hassall, 1908; Benedenia (Parabenedenia) hendor (von Linstow, 1889) Johnston, 1929 .

Material studied. USNPC: No. 35637 (voucher) (1 slide, 1 specimen) ex skin of unknown ®sh host from Spokane , Washington, USA .

Observations. This species was described by von Linstow (1889) from the scales, especially those on the belly, of Coryphaena hippurus (L.) from Chile. No type material was mentioned by von Linstow (1889) and we have been unable to trace any specimens from his work. Price (1938) redescribed B. hendor i based on a single specimen from an unknown ®sh species from Spokane, Washington, USA. We have examined this specimen, agree that it conforms to B. hendor i and oOEer the following information. Benedenia hendor i is a large species (e.g. ®gure 3A) at least 9 mm long and 5 mm wide. The haptor bears large accessory sclerites shaped like spear heads and an associated pair of tendons (®gure 21) as noted by von Linstow (1889). The anterior hamuli are longer than the accessory sclerites, their proximal ends just overlap the proximal ends of the accessory sclerites, but there is no overlap with the posterior hamuli (®gure 21). These morphological aspects of B. hendor i were not discussed by von Linstow (1889) but in his ®gures 2 and 3, he depicted the accessory sclerites as not overlapping the anterior hamuli. The posterior hamuli are relatively small and are located on the posterior border of the haptor. The marginal valve is much wider anteriorly and appears indented at each of the 14 hooklets.

The penis is strongly muscular and lies in a penis canal with little musculature in its walls. An accessory gland reservoir with thickened wall connects to the proximal end of the penis by a prominent duct, but no penis sac or similar muscularized organ encloses these structures.

Price (1938) described a slender`metraterm’ (5 uterus) but from the specimen we examined, this is best described as short because it enters the penis canal proximally. von Linstow (1889), however, described and drew a separate uterine duct extending the length of the penis complex and opening separately posterior to the male pore. Furthermore, von Linstow described no vagina for B. hendor i. von Linstow may have confused the vagina with the uterus. In the specimen we examined, we found no evidence for the arrangement proposed by von Linstow and conclude that this species probably possesses a common genital pore and separate vaginal pore. We did observe an internal fertilization chamber in the germarium.

Type-host and locality. Coryphaena hippurus (Coryphaenidae) , Caleta, Chile (von Linstow, 1889).

Published records. von Linstow (1889); Price (1938); Nikolaeva and Parukin (1968).

Descriptions. von Linstow (1889); Price (1938).

Published host records. Coryphaenidae : Coryphaena hippurus (see von Linstow, 1889; Nikolaeva and Parukin, 1968); unknown species ( Price, 1938).

Site . Skin.

Distribution. Caleta, Chile (von Linstow, 1889); Spokane, Washington, USA ( Price, 1938); Gulf of Mexico ( Nikolaeva and Parukin, 1968).

Remarks. von Linstow described a separate uterine pore for B. hendor i which is an unusual feature for Benedenia , is often di cult to observe and would, if con®rmed, place it with B. sciaenae and B. synagris . However he failed to observe a vagina and we think it likely that the uterus and the vagina were confused. To clarify these features, new material from the type-host, preferably from the typelocality, is needed to enable a complete reappraisal of this species. Presently, in the absence of further material, we agree with Price (1938) that the specimen from the Paci®c Coast of North America can be considered to be B. hendor i. As Price suggested, B. hendor i resembles closely B. seriolae . Price separated them only by the presence in B. seriolae of a band of vitelline follicles between the germarium and testes which is absent in B. hendor i, and by the shapes of the anterior hamuli which he claimed were more slender and not as curved in B. hendor i as in B. seriolae . The careful account of the reproductive system of B. seriolae by Kearn (1992) makes no mention of the band of vitellarium referred to by Price (1938). We regard the presence or absence of a band of vitelline follicles between the testes and germarium as a character of doubtful taxonomic value. Concerning the shapes of the hamuli, Price based his comparison on a single specimen of B. hendor i and diOEerences in orientation of the hamuli can account for large diOEerences in their apparent shape and size in capsalids ( Whittington and Horton, 1996). There is little doubt that B. hendor i and B. seriolae are related closely and an examination of further material may indicate that they are synonymous. The type-host of B. hendor i, C. hippurus , is distributed in the Atlantic, Indian and Paci®c Oceans ( Nelson, 1994) and investigations of this ®sh species for benedeniines in other localities are recommended. A Benedenia sp. was reported by Langdon (1991) from the cornea, skin and occasionally the gills of cultivated C. hippurus in Western Australia (table 8) when these ®sh had been in contact with yellowtail king®sh ( Seriola lalandi Valenciennes in Cuvier and Valenciennes) and samson ®sh ( S. hippos GuÈnther ). The former carangid species is a known host of B. seriolae (see p. 728). In view of the close similarity between B. hendor i and B. seriolae , a careful comparison of new benedeniine material from dolphin ®sh and from carangids is necessary to determine whether these Benedenia species are synonymous. We have been unable to obtain benedeniines from C. hippurus in Australia, but our quest will continue.

Figures

FIG. 16. Haptors of Yamaguti’s Hawaiian Benedenia species and B. epinepheli drawn to same scale from various specimens. (A) Benedenia bodiani; (B) B. epinepheli; (C) B. hawaiiensis; (D) B. lolo; (E) B. scari. Scale bar 5 250 Mm. Note tendon (te).