Schistorchis carneus Lühe, 1906

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 : 30-33

Schistorchis carneus Lühe, 1906

( Figs. 15–18 )

Host: White-spotted puffer (“Hadroom”), Arothron hispidus (Linnaeus) ( Tetraodontiformes : Tetraodontidae ).

Localities: Northern Red Sea, off Sharm El-Naga, Makadi Bay, Southern Hurghada, Egypt (26°55.16’N, 33°56.05’E– 26°53.59’N, 33°59.49’E; depth = 0.5–2.5 m; 17/December/2011); Northern Red Sea, off Safaga, Egypt (26°74’N, 33°95’E; depth = 5–30 m; 6/April/2017).

Site of infection: Lower & mid-intestine.

Deposited material: BM(NH) vouchers NHMUK 2017.9.28.12–30; 19 slides / 19 specimens .

Prevalence: 2 of 6 host specimens (33.3% infected).

Intensity: 9–28 worms/host specimen.

Mean intensity: 18.5 (37/2).

Relative density/abundance: 6.2 (37/6).

Re-description: [Based on 18 mature specimens. Measurements, morphometric percentages and morphometric ratios are given in Table 3] Worms blood red in color while live. Body plump, elongate to subelliptical in shape with almost parallel margins, maximum width near equatorial region either at posterior end of first 1/2 of body or anterior or posterior to this level by short distance. Anterior extremity rounded; posterior extremity more broadly rounded, at times almost truncate. Tegument thick and smooth, supported with several transverse tegumental folds along entire length of body. Forebody shorter than hindbody, less than 1/4 body length, gradually narrows near anterior end; hindbody wider than forebody, gradually narrows in posterior 1/5 of body. Pre-oral lobe absent to very short. Oral sucker spherical to subspherical, glandular/cellular, distinctly ventrosubterminal, “complex” type with margins of anterior musculature notched or indented (i.e. anterior circumoral lobes), very large at about 2¯3 times size of ventral sucker; mouth inconspicuous, rounded, directed anteroventrally, surrounded by strong semi-circular muscle fibers that sometimes cover mouth opening; partial Ushaped muscular sphincter half-encircling oral aperture posteroventrally. Ventral sucker pre-equatorial, situated at junction of first and second 1/4 of body, spherical to subspherical, sessile, unspecialized, smaller than oral sucker. Prepharynx absent. Pharynx transversally elliptical and often longitudinally compressed, smaller than suckers, muscular, weakly developed, often overlapped by oral sucker. Esophagus not observed. Intestinal bifurcation posterior to level of mid-forebody, about midway between suckers, separated from ventral sucker by small distance. Caeca two, simple, often filled with a dark material, wider and slightly arcuate posteriorly, equal in length, pass at some distance medial to lateral margins of worm to terminate at posterior extremity in small, separate ani.

Testes 11 (rarely fewer) (16 specimens [88.9%] with 11 testes distributed 5 left & 6 right; 1 specimen [5.6%] with 10 testes distributed 5 left & 5 right; 1 specimen [5.6%] with 7 testes distributed 2 left & 5 right), arranged in two straight or zigzag rows, smooth to slightly indented, sub-elliptical to sub-oval to irregular, either equal in size or some testes markedly different in size within a single individual, contiguous or separated from each other by short distance, occupy area between level of ovary and anterior region of second 1/2 of body, well-separated from posterior end. Post-testicular region about 1/3 to 1/2 of body length. Seminal vesicle saccate, conspicuous, large, transversally sub-spherical to elliptical, majority dextral to midline, distal portion narrower, confined to area between ovary and ventral sucker. Pars prostatica tubular, long, thin-walled, passes parallel to lateral margin of ventral sucker to about level of mid-sinistral rim of latter then unites with distal portion of metraterm to form hermaphroditic duct near anterior margin of ventral sucker; duct itself cylindrical, small, extends anterodorsally to ventral sucker. Prostatic cells well-developed, free in parenchyma, surrounds entire pars prostatica from junction with seminal vesicle to beginning of hermaphroditic duct. Genital pore median, opens immediately anterior to ventral sucker aperture or just anterior to sucker in forebody.

Ovary round to pyriform, smooth, in posterior portion of anterior 1/3 of body, submedian (dextral), either entirely pre-testicular or at level of anteriormost testes and between seminal vesicle and testes. Canalicular seminal receptacle variable in size (due to amount of sperm), sub-elliptical, sinistral or posterosinistral to ovary. Oötype median, directly sinistral to ovary and surrounded by large and conspicuous mass of Mehlis’ gland cells. Laurer’s canal arises from seminal receptacle, indistinct; distal portion not observed but expected to open dorsally. Oviduct proceeds from left margin of ovary, joined by duct from seminal receptacle, and passes into oötype. Vitellarium follicular; fields extend along lateral margins from as far anterior as mid-level of pharynx (occasionally begins at mid-level of ventral sucker) to posterior extremity, overlaps lateral margins of testes, confluent in post-testicular region; follicles numerous, small, sub-spherical to oval to irregular in shape, dorsal, ventral and lateral to caeca. Right and left transverse vitelline ducts immediately anterior to and unite at level of ovary forming small, median vitelline reservoir which opens through small duct into oötype complex. Uterus pre-testicular, short, coiled, intercaecal, in anterior hindbody, restricted to area between ovary, seminal vesicle, oötype complex, anteriormost left testis and genital pore, dorsally overlaps posterior edge of ventral sucker and extends anterosinistrally around left side of sucker. Metraterm tubular, short, wide, runs short distance parallel to pars prostatica and opens into hermaphroditic duct from left. Eggs numerous, operculate, oval, moderate in size, thin-shelled, non-filamented.

Excretory vesicle I-shaped, narrower posteriorly, median, extends to near beginning of second 1/3 of body, close behind or at level of anteriormost testes; two excretory ducts (i.e. collecting tubules) cross caeca ventrally, then run somewhat sinuously as far as oral sucker. Excretory pore terminal.

Remarks: Based on the diagnostic combination of characteristics given earlier, the present material belongs in the Megaperidae n. comb. within the Schistorchiinae ( Cribb & Bray 1999; Bray 2005a; Cribb 2005; Jones 2005; present study). In addition, the present specimens possess five or more testes (16 specimens with 11 testes, 1 specimen with 10 testes, 1 specimen with 7 testes) arranged in two rows and a “complex” type (i.e. highly cellular/ glandular) of oral sucker that is large in relation to body size as well as an elongate, sub-rectangular-shaped body, two caeca that open via separate ani, a long post-testicular region, a median genital pore at or above the anterior margin of the ventral sucker, and a marine tetraodontiform host—the white spotted puffer, A. hispidus ( Cribb 2005; present study). Therefore, we have placed these specimens in Schistorchis sensu stricto Lühe, 1906.

While there is the possibility that the present material may be an undescribed species, we have identified our specimens as S. carneus . Our material most closely resembles S. carneus in overall appearance, large size, the notched or indented anterior musculature of the oral sucker (i.e. anterior circumoral lobes), a median and immediately pre-acetabular genital pore, a relatively short distance between both suckers, and in many morphometric percentages and ratios ( Lühe 1906; Johnston 1913; Hafeezullah 1981; Table 3). We do note that our material differs from previous descriptions of S. carneus in a few features, the most striking of which is the anterior extent of the vitellarium and the appearance of the male genital system. In our material, the anteriormost extent of the vitellarium can be to the mid-level of the pharynx; whereas, the vitelline follicles of S. carneus as previously described are more variable in anterior extent: beginning at the level of either the ovary or the seminal vesicle ( Lühe 1906), the level of the ventral sucker ( Hafeezullah 1981) or the anterior border of the ventral sucker ( Johnston 1913)—not reaching the mid-level of the pharynx. While the seminal vesicle of S. carneus was rudimentarily described by Lühe (1906, Figs. 11 & 12) as lying in the median line just posterior to the ventral sucker, Johnston (1913, Fig. 11 ) and Hafeezullah (1981, Fig. 6) described this feature as being elongated and pearshaped, extending posterior to the ventral sucker from the left side and narrowing anteriorly to form a short pars prostatica; it is illustrated as a simple, medial, moderately-wide, oblong to clavate pouch. The saccate seminal vesicle of the present specimens of S. carneus is more conspicuous and larger in relation to overall body size, transversally sub-spherical to elliptical in shape and extends further dextral to the mid-line. The ovary is dextral as is the majority of the proximal seminal vesicle in our material and both features are opposite to the sinistromedial uterus (i.e. the majority of the seminal vesicle is at some distance from the uterus); whereas, in earlier descriptions of S. carneus , the ovary is either medial or a little to the right of the median line while the seminal vesicle lies almost wholly in the median plane making the majority of this feature closer to the uterus. We also noted that the egg length is slightly longer overall between earlier and current studies of this species (56–76 µm in previous S. carneus vs 64–88 µm in current S. carneus ) and the distal portion of the male system differs in size—the pars prostatica is longer and its length in relation to that of the hermaphroditic duct is greater in our specimens than in previously-described S. carneus (see Table 3). Finally, while S. carneus parasitizes Arothron spp. ( A. stellatus & A. hispidus ), the geographic localities between previous and current studies of this digenean are considerably distant (off Sri Lanka and Australia vs off the coast of Egypt in the Red Sea). We attribute these minor differences to a combination of intraspecific variability (e.g. we noted that the anterior extent of the vitellarium in previous descriptions of S. carneus was highly variable; there is overlap in egg lengths) and possible variation in the quantity of sperm within the seminal vesicle (i.e. the overall arrangement of the ovary and seminal vesicle is the same between our material and earlier descriptions of S. carneus relative to the uterus, including the orientation - either dextral or sinistral of midline). Furthermore, if a host species ( A. hispidus ) can occur very widely—and this one does (see Froese & Pauly 2017)—why not their parasites? Indeed, it is believed that we do not yet really understand the distribution of trematode species in the Indo-Pacific (Dr. Tom Cribb, Univ. of Queensland—pers. comm.).

With the re-description of S. carneus herein as well as the detailed comparisons of our material to earlier descriptions of this and other species of Schistorchis sensu stricto ( Table 3), we can now provide an updated generic diagnosis for Schistorchis sensu stricto and offer a key to the four species we recognize in this genus.

Figures

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 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.