Schistorchiinae Yamaguti, 1942

Blend, Charles K., Karar, Yasser F. M. & Dronen, Norman O., 2017, Revision of the Megaperidae Manter, 1934 n. comb. (Syn. Apocreadiidae Skrjabin, 1942) including a reorganization of the Schistorchiinae Yamaguti, 1942, Zootaxa 4358 (1), pp. 1-44 : 10-13

Subfamily Schistorchiinae Yamaguti, 1942

(Syn. Sphincterostomatinae Yamaguti, 1958 )

Diagnosis. (Based on Cribb 2005 and present study) Body oval to linguiform to elongate, can be moderately large. Tegument spinous or unarmed. Eye-spot pigment present or absent. Oral sucker subterminal or terminal, muscular or glandular/cellular and can be quite large, with or without circumoral lobes, partial U-shaped sphincter half encircling oral aperture posteroventrally. Ventral sucker pre-equatorial, smaller or larger than oral sucker. Prepharynx very short or lacking. Pharynx poorly to well-developed. Esophagus short or absent. Intestinal bifurcation in forebody. Caeca end blindly, open through ani or form uroproct. Testes two to multiple (five or more) in number, tandem or opposite, can occur in one or more rows, smooth to lobed, primarily post-ovarian, in hindbody. Cirrus pouch absent. Seminal vesicle saccate or tubular. Pars prostatica present; prostatic cells free in parenchyma. Genital pore median to submedian, immediately anterior to or just overlapped by anterior margin of ventral sucker. Ovary round to subglobular, smooth, in hindbody or at level of ventral sucker, median to submedian, pre-testicular. Canalicular seminal receptacle and Mehlis’ gland present. Laurer’s canal present. Vitellarium follicular; follicles extensive, may be restricted to hindbody or enter forebody. Uterus restricted to area proximate to ventral sucker and either ovary or anterior testis/testes, distal loops can extend more anteriorly. Eggs medium to very large in size. Excretory vesicle I-shaped, extend to level of testes; primary excretory ducts (i.e. collecting tubules) can reach level of oral sucker; excretory pore terminal or subterminal. Adults in intestine of marine fishes; Indian and Pacific Oceans and Red Sea.

Type genus. Schistorchis Lühe, 1906 (Syn: Megacreadium Nagaty, 1956 ).

Remarks. Members of the Schistorchiinae are unique within the Megaperidae n. comb. in possessing a genital pore anterior to the ventral sucker and an oral sucker with a partial U-shaped sphincter half encircling the oral aperture posteroventrally. The main features used to distinguish the five recognized genera of schistorchiines include the number of testes, the terminal nature of the caeca (ending in ani, uroproct or blindly) and oral sucker morphology ( Cribb 2005).

Sphincteristomum was erected with the description of Sphincteristomum acollum Oshmarin, Mamaev & Parukhin, 1961 infecting the intestine of the starry triggerfish, Abalistes stellaris (Bloch & Schneider) ( Tetraodontiformes : Balistidae ), from the Gulf of Tonkin off northern Vietnam ( Oshmarin et al. 1961). Sphincterostoma was erected by Yamaguti (1937) with the description of Sphincterostoma branchiostegi Yamaguti, 1937 collected from the intestine of the horsehead tilefish, Branchiostegus japonicus (Houttuyn) ( Perciformes : Malancanthidae), from the Sea of Japan. Both genera are distinguished from other schistorchiines by possessing two testes instead of multiple testes (5–7 or more) ( Cribb 2005; present study). Species of either Sphincteristomum or Sphincterostoma are differentiated by the former possessing caeca that open independently via separate ani and a highly glandular oral sucker while the latter possesses caeca that unite and open via a uroproct and a muscular (not glandular) oral sucker (see our comments below regarding the glandular vs muscular oral sucker in schistorchiines). We consider Sphincteristomum and Sphincterostoma to be unique and, thus, recognize herein both schistorchiine genera.

At least twelve species have been assigned at one time or another to Schistorchis , the type genus of the Schistorchiinae . Currently, Cribb & Gibson (2017a) recognize eleven species in this genus. Johnston (1913) established Pleorchis oligorchis Johnston, 1913 from the intestine of the white-spotted puffer, Arothron hispidus (Linnaeus) (= Tetrodon hispidus Linnaeus ) ( Tetraodontiformes : Tetraodontidae ), from off Queensland, Australia, and described the oral sucker of this species as very large and strong with a terminal and comparatively small opening (i.e. mouth) surrounded by a “condensation of the tissues round its edge so that the latter is specially tough” (see Figs. 11 & 38 of Johnston 1913). Odhner (1928) (also see Price 1932, p. 8; Hafeezullah 1981, p. 175) synonymized P. oligorchis with S. carneus , the type species of Schistorchis , originally described by Lühe (1906) from Arothron (= Tetrodon ) stellatus ( Tetraodontiformes : Tetraodontidae ), from off Sri Lanka. (We noted that later works by Yamaguti [1942, 1958, 1971] recognized that P. oligorchis belonged within Schistorchis [as Schistorchis oligorchis ( Johnston, 1913) Yamaguti, 1942 ], but he did not consider S. oligorchis to be conspecific with S. carneus .) Hafeezullah (1981) collected S. carneus from the intestine of A. hispidus obtained off Mandapam, India, which is across the relatively narrow Gulf of Manaar from Sri Lanka. The oral sucker of this material was described by Hafeezullah (1981, Fig. 6) as possessing a small mouth surrounded by strong circular muscles that sometimes covered the mouth opening, the anterior margin of the sucker appeared notched, lobed or indented, and the remainder of this feature was highly cellular in appearance. Hafeezullah (1981) also re-described S. skrjabini from the intestine of the short-nosed tripodfish, Triacanthus biaculeatus (Bloch) (= Triacanthus brevirostris Temminck & Schlegel ) ( Tetraodontiformes : Triacanthidae ), from the Vellar Estuary at Porto-Novo (=Parangipettai) located off the Coromandal coast of southeast India in the Bay of Bengal. Schistorchis skrjabini originally had been described from the North Vietnamese Bay by Parukhin (1963) parasitizing the intestine of two fish species: the starry triggerfish, Abalistes stellaris (Bloch & Schneider) ( Tetraodontiformes : Balistidae ), and T. biaculeatus (as T. brevirostris ) (see Table 1). While Parukhin (1963, Fig. 1 ) offered only the dimensions of the oral sucker (280–340 µm × 300–320 µm)—fairly large in relation to the entire worm—Fig. 1 clearly shows a band of circular muscles surrounding the mouth. Hafeezullah (1981, Figs. 4 & 5) provided more details stating that the oral sucker differentiated into a smaller muscular part sometimes with muscular lips or small lobes around the mouth while the rest of the sucker appeared highly cellular. Based on the work by Hafeezullah (1981), our morphological comparisons of published type descriptions, examination of oral sucker photographs taken from type and voucher specimens of recognized species of Schistorchis sent to us from the HWML, MPM, USNM and ZSI as well as observations of new materials obtained for this study, we discerned the oral sucker in species of Schistorchis to have two distinct morpho-types. One is a “complex” type, usually quite large in relation to body size, containing strong circumoral muscles and anteriorly- or posteriorly-directed lobes localized immediately around and sometimes covering the mouth with the remainder of the oral sucker demonstrating a highly cellular/glandular appearance. The other morpho-type of oral sucker is a “simple” type, not as large, with no circumoral lobes and that is entirely muscular as opposed to highly cellular/glandular in appearance. A partial U-shaped sphincter half encircling the oral aperture posteroventrally is present in both “ types ” of oral suckers—characteristic of all members of the Schistorchiinae .

The type and only species of Neomegacreadium , Neomegacreadium okinawanum Machida & Kuramochi, 1999 , was described from the intestine of the threetooth puffer, Triodon macropterus Lesson ( Tetraodontiformes : Triodontidae ), collected off Nago, Okinawa Prefecture, Japan ( Machida & Kuramochi 1999). This genus was distinguished from Megacreadium (discussed immediately below) by having a mouth enclosed by a broad muscular lobe anteriorly and a well-developed muscular bundle posterolaterally (see Fig. 17 of Machida & Kuramochi 1999), a uroproct, ten (occasionally 11 or 12) testes, vitellarium extending to the posterior level of the oral sucker and an egg 59–71 µm × 40–50 µm in size. With this diagnostic combination of testes number (usually 10–12), an oral sucker that is muscular (see Cribb 2005, p. 639 where the oral sucker of Neomegacreadium is described as “normally muscular”) and lacks a highly cellular/glandular appearance, and caeca that open via a uroproct, we consider Neomegacreadium to be unique and, thus, recognize herein this schistorchiine genus.

In the type and only species of Megacreadium , M. tetrodontis , the oral sucker is large and globular, highly cellular, and surrounding the mouth are two large muscular, lateral lobes and one smaller, median, posterior lobe, each scalloped or frilled with short processes ( Nagaty 1956). Hafeezullah (1981) compared the morphology of the circumoral muscular lobes within the oral suckers of S. carneus and S. skrjabini to that of M. tetrodontis and concluded that the latter species differed from the former two only in the degree of indentation within this feature; therefore, there appeared evidence for considering Megacreadium a junior synonym of Schistorchis (see also Sogandares-Bernal & Hutton 1959, p. 59, who considered Megacreadium to be a synonym of Schistorchis ). Cribb (2005) recognized both genera and used oral sucker morphology in his key to the genera of the Schistorchiinae to distinguish species of Megacreadium (oral sucker highly glandular [i.e. “complex” type]) from those of Schistorchis (oral sucker normally muscular [not glandular] [i.e. “simple” type]; also see Cribb & Bray 1999, p. 6). In the generic diagnosis of Megacreadium, Cribb (2005) referred to the oral sucker as highly glandular (i.e. cellular) with a reduced musculature—consistent with the observations of Hafeezullah (1981) regarding the nature of the oral sucker in S. carneus and S. skrjabini (see above). Testes number has also been another point of ambiguity in comparative analyses of both genera. In the description of P. oligorchis (= S. carneus ), Johnston (1913) noted variability in testes number (5–11) in eleven mature specimens observed; whereas, Lühe (1906, Figs. 11 –12) and Hafeezullah (1981, Fig. 6) each recorded 11 testes for their specimens of S. carneus . Eight testes were counted in the one mature specimen of M. tetrodontis observed by Nagaty (1956). As far as we are aware, there has been no re-description of M. tetrodontis , and given that the type description by Nagaty (1956) was based on only a single specimen of M. tetrodontis (i.e. impossible to observe intraspecific variability), we cannot rule out the possibility that additional specimens of this species may exhibit a variable number of testes. Cribb (2005) included eight testes as a diagnostic character in the generic diagnosis of Megacreadium and “usually about 11” testes as a diagnostic character for species of Schistorchis . However, we noted that Fig. 47.20 of Cribb (2005, p. 638) illustrated an unidentified specimen of Megacreadium from the orange-lined triggerfish, Balistapus undulatus (Park) ( Tetraodontiformes : Balistidae ), collected off Heron Island, southern Great Barrier Reef, Australia; this illustrated specimen contains 13, not 8, testes (i.e. testes number in species of Megacreadium [8 & 13] can overlap testes number in species of Schistorchis [~11]). Based on Johnston (1913) and our observations in the present study, we believe overall testes number (and the number of testes per row, where applicable) to exhibit too high a degree of plasticity to be an effective diagnostic characteristic distinguishing both genera (also see Hafeezullah 1981, p. 176). Furthermore, based on the conclusions of Sogandares-Bernal & Hutton (1959) and Hafeezullah (1981) regarding the similar oral sucker morphologies of S. carneus , S. skrjabini and M. tetrodontis , the type description of the oral sucker of M. tetrodontis , the recognition by Cribb (2005) of the “complex” nature of the oral sucker (i.e. “reduced musculature, highly glandular”) in Megacreadium , and the new observations we make herein (see below), we support the earlier authors who declared Megacreadium to be a junior synonym of Schistorchis and hereby re-assign Megacreadium tetrodontis Nagaty, 1956 to Schistorchis as Schistorchis tetrodontis ( Nagaty, 1956) n. comb.

Schistorchis tetrodontis n. comb. and three of the eleven species of Schistorchis acknowledged by Cribb & Gibson (2017a) — S. carneus , S. paruchini and S. skrjabini —differ from the eight remaining species of Schistorchis by possessing the following diagnostic combination of characters: a unique “complex” (i.e. highly cellular/ glandular) type of oral sucker that is quite large in relation to body size; an elongate, somewhat sub-rectangularshaped body; 5+ testes arranged in at least two rows; caeca that open via separate ani; a long post-testicular region; a median genital pore at the anterior margin of or just anterior to the ventral sucker; and these four species of Schistorchis parasitize the intestine of marine fish within the Order Tetraodontiformes ( Nagaty 1956; Table 1). Schistorchis paruchini , thus far not discussed in detail, was described by Kurochkin (1974) from a single specimen found in the intestine of the southern leatherjacket, Meuschenia australis (Donovan) (= Navodon australis [Donovan]) ( Tetraodontiformes : Monacanthidae ), collected in the Great Australian Bight. While attempts were unsuccessful in obtaining photographs of the oral sucker of the holotype specimen of this species (Accession No. GT-70269 - deposited in the Laboratory of Parasitology of Marine Animals, Pacific Research Institute of Fisheries & Oceanography [TINRO], Vladivostok, Russia), Kurochkin (1974, p. 67) provided a diameter measurement for the oral sucker (660 µm mounted, 880 µm while living) as well as an illustration. This illustration revealed neither strong circumoral muscles around the mouth nor the presence of a partial U-shaped sphincter half encircling the oral aperture posteroventrally—characteristic of members of the Schistorchiinae . We could not ascertain the glandular/cellular nature (i.e. “complex” type) of the remainder of the sucker, but we did note the large size of the sucker relative to the body and the unusually distorted shape of the mouth illustrated for S. paruchini which was reminiscent of S. skrjabini as illustrated by Hafeezullah (1981, Figs. 4 & 5); perhaps indicative of a muscular area localized around the mouth (sans muscular lips or small lobes) and a highly glandular/cellular appearance. As seen earlier with S. tetrodontis n. comb., it is impossible to observe any intraspecific variability for S. paruchini (i.e. described from a single worm); however, intraspecific variability in the oral sucker of other accepted species of Schistorchis has been observed (e.g. the re-descriptions by Hafeezullah 1981, Figs. 4 –6 of S. carneus and S. skrjabini compared to the type descriptions by Lühe 1906 and Parukhin 1963 of these species) and the new observations in our present study also showed this variability (see below). Based on this possibility as well as the strong similarities between S. paruchini and S. carneus , S. skrjabini and S. tetrodontis n. comb. as related to the diagnostic combination of characters listed earlier, we believe these four species comprise the valid species of Schistorchis sensu stricto (type species— S. carneus ).

The remaining eight species of Schistorchis (see Cribb & Gibson 2017a and Table 1) all differ from the four species of Schistorchis sensu stricto in possessing a “simple” type of oral sucker that is smaller in relation to body size, lacks circumoral lobes, and is entirely muscular as opposed to highly cellular/glandular in appearance. Of these, S. longivesiculurus , S. seychellesiensis , S. stenosoma and S. zancli have caeca that end in separate ani while the caeca in S. callyodontis , S. haridis , S. manteri and S. sigani end blindly. Based on our experience working with a variety of digeneans from many families, we have noted that researchers often consider the presence/absence of a cyclocoel, uroproct, ani and/or blindly-ending caeca to be a generic-level character (see Cribb 2005). Given this, we believe it is best to erect two new genera for these eight species: Paraschistorchis n. gen. represents those former Schistorchis species with a “simple” oral sucker and caeca that end in separate ani while Plesioschistorchis n. gen. contains those former Schistorchis species with a “simple” oral sucker and caeca that end blindly.

Figures

FIGURES 4¯6. Plesioschistorchis haridis (Nagaty, 1957) n. comb. (Megaperidae n. comb.: Schistorchiinae) from the common parrotfish, Scarus psittacus Forsskål (Scaridae), from the Red Sea off Egypt. 4. Adult specimen, ventral view. 5. Terminal genitalia, ventral view. 6. Oval eggs. Abbreviations: Ce, Cecum; GP, Genital pore; HD, Hermaphroditic duct; Me, Metraterm; OS, Oral sucker; Ov, Ovary; PC, Prostatic cells; Ph, Pharynx; PP, Pars prostatica; SR, Seminal receptacle; SV, Seminal vesicle; Te, Testes; Ut, Uterus; VD, Vitelline duct; VF, Vitelline follicles; VR, Vitelline reservoir; VS, Ventral sucker.

FIGURES 11¯12. Plesioschistorchis callyodontis (Yamaguti, 1942) n. comb. and Plesioschistorchis manteri (Gupta & Tandon, 1984) n. comb. 11. P. callyodontis ventral view of adult redrawn from Yamaguti (1942, Fig. 15). 12. P. manteri ventral view of adult redrawn from Gupta & Tandon (1984, Fig. 1). Abbreviations: Ce, Cecum; EA, Excretory arm/duct; EP, Excretory pore; Es, Esophagus; EV, Excretory vesicle; GP, Genital pore; HD, Hermaphroditic duct; LC, Laurer’s canal; Me, Metraterm; MG, Mehlis’ gland; Oo, Oötype; OS, Oral sucker; Ov, Ovary; PC, Prostatic cells; Ph, Pharynx; PP, Pars prostatica; SR, Seminal receptacle; SV, Seminal vesicle; Te, Testes; Ut, Uterus; VD, Vitelline duct; VF, Vitelline follicles; VR, Vitelline reservoir; VS, Ventral sucker.

FIGURES 1–3. Plesioschistorchis callyodontis (Yamaguti, 1942) n. comb. (Megaperidae n. comb.: Schistorchiinae) from the common parrotfish, Scarus psittacus Forsskål (Scaridae), from the Red Sea off Egypt. 1. Adult specimen, ventral view. 2. Terminal genitalia, ventral view. 3. Elliptical eggs. Abbreviations: Ce, Cecum; EA, Excretory arm/duct; EP, Excretory pore; EV, Excretory vesicle; GP, Genital pore; HD, Hermaphroditic duct; Me, Metraterm; OS, Oral sucker; Ov, Ovary; PC, Prostatic cells; Ph, Pharynx; PM, Parenchymal mass of cells; PP, Pars prostatica; SR, Seminal receptacle; SV, Seminal vesicle; Te, Testes; Ut, Uterus; VF, Vitelline follicles; VS, Ventral sucker.

FIGURES 15–18. Schistorchis carneus Lühe, 1906 (Megaperidae n. comb.: Schistorchiinae) from the white-spotted puffer, Arothron hispidus (Linnaeus) (Tetraodontidae), from the Red Sea off Egypt. 15. Composite of whole adult specimen, ventral view. 16. Composite of terminal genitalia, ventral view. 17. Composite of proximal female complex, ventral view. 18. Hindbody revealing anterior extent of excretory vesicle and termination of caeca, ventral view. Abbreviations: An, Anus; EA, Excretory arm/duct; Eg, Eggs; EP, Excretory pore; EV, Excretory vesicle; GP, Genital pore; LIC, Left intestinal cecum; Me, Metraterm; MG, Mehlis’ gland; OD, Ovarian duct; Oo, Oötype; OS, Oral sucker; Ov, Ovary; PC, Prostatic cells; Ph, Pharynx; PP, Pars prostatica; RIC, Right intestinal cecum; SR, Seminal receptacle; SV, Seminal vesicle; Te, Testes; Ut, Uterus; VD, Vitelline duct; VF, Vitelline follicles; VR, Vitelline reservoir; VS, Ventral sucker.