Plesioschistorchis haridis ( Nagaty, 1957 ) Blend & Karar & Dronen, 2017

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 : 21-25

Plesioschistorchis haridis ( Nagaty, 1957) n. comb.

( Figs. 4 –6)

(Syn. Schistorchis haridis Nagaty, 1957 )

Host: Common parrotfish (“Ghabban”), Scarus psittacus Forsskål ( Perciformes : Scaridae ).

Locality: El-Halaka Fish Market, Hurghada, Egypt (27°23.28’N, 33°84.08’E; 25/August/2015 [fish believed to have been obtained in northern Red Sea]).

Site of infection: Lower intestine.

Deposited material: BM(NH) vouchers NHMUK 2017.9.28.1–9; 9 slides / 9 specimens .

Prevalence: 6 of 8 host specimens (75% infected).

Intensity: 3−7 worms/host specimen.

Mean intensity: 3.83 (23/6).

Relative density/abundance: 2.88 (23/8).

Re-description: [Based on 9 specimens. Measurements, morphometric percentages and morphometric ratios are given in Table 2]. Body plump, elongate with parallel margins, maximum width at junction of first and second 1/5 of body (i.e. at level of ventral sucker). Anterior extremity rounded; posterior extremity less rounded, slightly truncated in several specimens. Tegument smooth. Forebody gradually attenuated; hindbody wider than forebody, gradually narrows in posterior 1/3 of body. Pre-oral lobe short and distinct. Oral sucker spherical to subspherical, muscular, distinctly ventro-subterminal, “simple” type with no anterior circumoral lobes; mouth conspicuous, rounded, directed anteroventrally; partial U-shaped muscular sphincter half-encircling oral aperture posteroventrally. Ventral sucker pre-equatorial, situated at junction of first and second 1/5 of body, spherical to subspherical, sessile, unspecialized, slightly larger than oral sucker. Numerous parenchymal cells concentrated around outer margin of ventral sucker, especially its posterior edge. Prepharynx not observed. Pharynx transversely oval to dolioform, smaller than suckers, muscular, well-developed. Esophagus indistinct, very short, straight, broad. Intestinal bifurcation immediately posterior to level of mid-forebody, separated from ventral sucker by short distance. Caeca two, simple, narrow to moderately wide, slightly arcuate posteriorly, left caecum often slightly longer than right caecum, pass along lateral margins of worm to terminate blindly at posterior extremity; ani absent.

Testes 11, arranged in one zigzag or straight row, smooth, elliptical to oval, equal in size but anteriormost testis often larger than others, well-separated from each other, occupy area between ovary and middle of posterior 1/5 of body. Post-testicular region small. Seminal vesicle distinct (especially in lateral view), large, long, bipartite; saccate proximal portion median to submedian (sinistral), extends anteriorly in acute angle from level just posterior to ovary to near level of posterosinistral edge of ventral sucker then tapers to form tubular distal portion which passes parallel to sinistral margin of ventral sucker to level anterior to mid-point of sucker, all within second half of first 1/3 of body. Pars prostatica sub-elliptical, short, thick-walled, extends a short distance anterosinistrally around left margin of ventral sucker then unites with distal portion of metraterm to form hermaphroditic duct; duct itself sub-elliptical, large, moderate in length, thick-walled, continues anterosinistrally around left margin of ventral sucker. Prostatic cells well-developed, free in parenchyma, a condensed mass distributed around pars prostatica and distal portions of seminal vesicle and metraterm. Genital pore submedian, immediately anterosinistral to ventral sucker, may ventrally overlap left caecum.

Ovary round, smooth, in anterior hindbody and in posterior portion of anterior 1/3 of body, median to submedian (dextral), pre-testicular and separated from anterior testis, dextral to proximal portion of seminal vesicle. Canalicular seminal receptacle sub-elliptical, smaller than ovary, extends anterior or anterosinistral to or overlaps ovary. Oviduct proceeds from left margin of ovary to enter oötype located immediately sinistral or posterosinistral to ovary. Mehlis’ gland cells large, conspicuous. Distal portion of Laurer’s canal not observed but expected to open dorsally. Vitellarium follicular; fields extend along lateral margins from mid-level of ovary (relatively far posterior to ventral sucker) to posterior extremity, right lateral band of follicles often extends further anterior than left lateral band; overlaps lateral margins of testes, confluent in post-testicular region; follicles numerous, small, sub-spherical to oval, dorsal, ventral and lateral to caeca. Right and left transverse vitelline ducts unite and form small vitelline reservoir short distance posterior to ovary. Uterus pre-testicular, short, few coils, intercaecal, in anterior hindbody and restricted to area between mid-level of ovary and genital pore, proximal portion overlaps distal, tubular portion of seminal vesicle and posterior margin of ventral sucker before it passes anterosinistrally around left margin of ventral sucker. Metraterm tubular, runs anteriorly along left side of pars prostatica and joins distal portion of latter to form hermaphroditic duct. Eggs numerous, operculate, oval, moderate in size, thin-shelled, non-filamented.

Excretory vesicle I-shaped, moderately narrow, median, extends to equatorial region or just anterior and proximate to anteriormost testis; two primary excretory ducts (i.e. collecting tubules) extend anteriorly into forebody. Excretory pore terminal.

Remarks: Specimens of the two newly-collected species re-described above were assigned to the Megaperidae n. comb. and the Schistorchiinae based on the following combination of diagnostic features shared: no circumoral crown of spines, proboscides or ridge; the presence of a pharynx, oral and ventral sucker; an oral sucker with a partial U-shaped sphincter half encircling the oral aperture posteroventrally; no cirrus pouch; testes that are not elongate and located in the hindbody; the absence of both a hermaphroditic sac and a thickened wall in the distal portion of the male duct; a genital pore located anterior to the ventral sucker; follicular vitellarium; an Ishaped excretory vesicle; an excretory pore located at the posterior extremity; and both species infect the intestine of a marine teleost host (the common parrotfish, S. psittacus ) ( Cribb & Bray 1999; Bray 2005a; Cribb 2005; Jones 2005; present study). Additionally, the presence of five or more testes (11 most frequent number), 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, and caeca that end blindly place both species in Plesioschistorchis n. gen. A comparison of this material to previously described species of Schistorchis sensu lato allowed us to positively identify our material as two species we now consider to belong in Plesioschistorchis n. gen.: Plesioschistorchis callyodontis ( Yamaguti, 1942) n. comb. (Syn. Schistorchis callyodontis Yamaguti, 1942 ) and Plesioschistorchis haridis ( Nagaty, 1957) n. comb. (Syn. Schistorchis haridis Nagaty, 1957 ) ( Yamaguti 1942; Nagaty 1957; Cribb 2005; present study).

As far as we know, there are only three descriptions of either species in the literature (see Table 2). Yamaguti (1942) originally described P. callyodontis n. comb. (as Schistorchis callyodontis ) from a single specimen infecting the intestine of an unidentified parrotfish species ( Callyodon Gronow—Perciformes : Scaridae ) from off Naha, Japan. Nagaty & Abdel-Aal (1962) re-described this species based on 10 of 48 specimens they found parasitizing the intestine of the blue-barred parrotfish, Scarus ghobban Forsskål (= Callyodon ghobban [Forsskål] & Callyodon guttatus [Bloch & Schneider]), and the redtail parrotfish, Sparisoma chrysopterum (Bloch & Schneider) (= Scarus chrysopoma Bloch & Schneider ) ( Perciformes : Scaridae ), collected off Hurghada, Egypt, in the Red Sea. Plesioschistorchis haridis n. comb. was originally described as Schistorchis haridis by Nagaty (1957) based on 11 specimens found in the intestine of the Candelamoa parrotfish, Hipposcarus harid (Forsskål) (= Pseudoscarus harid Forsskål ) ( Perciformes : Scaridae ), also from off Hurghada, Egypt, in the Red Sea.

Our specimens of P. callyodontis n. comb. compare favorably in overall appearance and in most allometric measurements with the original description of S. callyodontis by Yamaguti (1942, Fig. 15 ) and/or the re-description of this species by Nagaty & Abdel-Aal (1962, Fig. 1 ). We noted a few relatively minor differences between our specimens and the previous descriptions of P. callyodontis n. comb. (= S. callyodontis ). The large mass of parenchymal cells that are concentrated around the outer margin of the ventral sucker appeared more condensed and distinct in our material. The saccate, proximal portion of the seminal vesicle of the worms from S. psittacus extends anteriorly in a longitudinal direction; whereas, this same feature within the worms earlier found in Callyodon sp., S. ghobban and S. chrysopterum extends anteriorly in a more transverse direction between the ventral sucker and ovary. We further noted in our specimens a shorter esophagus, a larger pharynx: oral sucker length ratio, a more variable testes number (5 & 11), a longer pars prostatica and hermaphroditic duct, and a relatively shorter forebody, pharynx, distance between suckers, seminal vesicle, pre-bifurcal and pre-genital pore distance as well as a longer distance between the ventral sucker and both the ovary and closest testis in relation to overall body length ( Table. 2). Our specimens of P. haridis n. comb. also are very similar in appearance and allometry to the original description of S. haridis by Nagaty (1957, Fig. 1 ); however, we noted a few minor differences between both sets of conspecific specimens. Nagaty (1957) mentioned that P. haridis has a seminal vesicle that is dorsal to the ventral sucker, while in the present material, it extends anteriorly from a level just posterior to the ovary to near the posterosinistral edge of the ventral sucker, then the seminal vesicle tapers to form a tubular distal portion which passes parallel to the sinistral margin of the ventral sucker up to a level anterior to the mid-point of it. The present material from S. psittacus also exhibits a greater distance between both the ventral sucker and ovary to the closest testis, smaller post-testicular, post-caecal and post-vitelline regions in relation to the overall body length and the length and width ratios of the pharynx to the ventral sucker are larger when compared to P. haridis n. comb. from H. harid ( Table. 2).

The present specimens of P. haridis n. comb. & P. callyodontis n. comb. re-described herein were collected from the same host species ( S. psittacus ), the same locality (off Hurghada, Egypt, in the Red Sea), and are close in overall appearance; however, we noted some differences between both species in our material, especially in the extent and appearance of the genital systems. In P. callyodontis n. comb., the testes are variable in number (5 & 11), arranged in two zigzag rows, and the posterior extent of the testes is to about the middle of the posterior 1/3 of the body, while in P. haridis n. comb. the testes have a constant number (11), arranged in one straight or zigzag row, and the posterior extent of the testes is to about the middle of the posterior 1/5 of body. The seminal vesicle in P. callyodontis n. comb. is large, clavate to pyriform, rounded proximally and tapering distally, extending in an obliquely vertical direction between the ventral sucker and ovary in the anterior portion of the second 1/4 of the body; whereas, the seminal vesicle of P. haridis n. comb. is large, long, and differentiated into two parts within the second half of the first 1/3 of the body: the proximal part is saccate, sinistromedial and extends in an obliquely vertical direction from a level just posterior to the ovary to a level near the posterosinistral edge of the ventral sucker then tapers forming a long, tubular distal part which passes parallel to the sinistral margin of the ventral sucker reaching to above the mid-point of it. Plesioschistorchis callyodontis n. comb. possesses a pars prostatica that is sub-cylindrical and thin-walled, its hermaphroditic duct is tubular and narrow, and the genital pore is median and immediately anterior to the ventral sucker—not overlapping the caeca. In P. haridis n. comb., the pars prostatica is sub-elliptical and thick-walled, its hermaphroditic duct is large, sub-elliptical and thick-walled, and the genital pore is submedian and immediately anterosinistral to the ventral sucker, at times overlapping the left caecum. Another difference is that P. callyodontis n. comb. has an ovary that is median, separated from the anteriormost testis by a short distance, dextral to the seminal receptacle and situated in the posterior portion of the anterior half of the body; however, P. haridis n. comb. has a dextromedial ovary that is separated from the anterior testis by a relatively long distance, dextral to the proximal portion of the seminal vesicle and situated in the posterior portion of the anterior 1/3 of the body. The seminal receptacle of P. callyodontis n. comb. is oblong to retort-shaped, as large as the ovary or larger and extends obliquely between the ovary and the anteriormost testes, yet in P. haridis n. comb., the seminal receptacle is sub-elliptical, smaller than the ovary and extends anterior or anterosinistral to or overlaps the ovary. Plesioschistorchis callyodontis n. comb. has a longer and more coiled uterus than observed in P. haridis n. comb. The two suckers in P. callyodontis n. comb. are either equal in size or the oral sucker is slightly larger than the ventral sucker; whereas, in P. haridis n. comb., the ventral sucker is larger than the oral sucker. Morphometrically, P. callyodontis n. comb. differs from P. haridis n. comb. (see Table. 2) in possessing a ventral sucker conspicuously further distant from both the ovary (20.0%−21.8% of body length in P. callyodontis n. comb. vs 0.8%−3.7% of body length in P. haridis n. comb.) and the closest anterior testis (23.6%−24.4% vs 9.0%−13.7%), a shorter seminal vesicle length (11.0%−11.4% vs 15.8%−22.6%), a shorter postuterine distance (54.0%−54.2% vs 66.8%−71.1%), and a longer pre-ovarian distance (43.7%−45.3% vs 24.7%−34.4%).

Given the additional observations and measurements included herein ( Table 2) from the re-descriptions of Plesioschistorchis callyodontis n. comb. and Plesioschistorchis haridis n. comb. (Syns. Schistorchis callyodontis , Schistorchis haridis )—both obtained from the common parrotfish ( S. psittacus ), an undocumented host for either species—we now present keys to the four species each we recognize in Paraschistorchis n. gen. and in Plesioschistorchis n. gen.

Key to species of Paraschistorchis n. gen. a

1a. Oral sucker rounded to elliptical........................................................................ 2.

1b. Oral sucker funnel-shaped to subquadrate........................... Paraschistorchis zancli ( Hanson, 1953) n. comb. (Syn. Schistorchis zancli Hanson, 1953 ) ( Fig 7 ).

2a. Seminal vesicle saccular; oral sucker larger than ventral sucker................................................ 3.

2b. Seminal vesicle long, winding, tubular with thick muscular walls; suckers about equal in size........................................................................... Paraschistorchis longivesiculurus ( Hafeezullah, 1981) n. comb. (Syn. Schistorchis longivesiculurus Hafeezullah, 1981 ) (Fig. 8).

3a. Anterior extent of vitelline follicles to level of posterior margin of ventral sucker or slightly posterior to it (i.e. at level of ovary which is itself close to ventral sucker); testes transversally elongated (testis width 2 times its length or more); egg 43–48 × 35– 40................................................... Paraschistorchis seychellesiensis ( Toman, 1989) n. comb. (Syn. Schistorchis seychellesiensis Toman, 1989 ) ( Fig. 9 ).

3b. Anterior extent of vitelline follicles to level far posterior to ventral sucker (i.e. posterior to ovary which is itself far from ventral sucker); testes rounded to elliptical; egg 51–56 × 31–36........ Paraschistorchis stenosoma ( Hanson, 1953) n. comb. (Syn. Schistorchis stenosoma Hanson, 1953 ) (Fig. 10).

Key to species of Plesioschistorchis n. gen. a

1a. Anterior extent of vitelline follicles to level of posterior margin of ventral sucker or slightly posterior to it.............. 2.

1b. Anterior extent of vitelline follicles to level far posterior to ventral sucker (i.e. at level of ovary or a short distance anterior to it) ................................................................................................ 3.

2a. Genital pore median; egg ellipsoidal or oval, 69–81 × 36–42.... Plesioschistorchis callyodontis ( Yamaguti, 1942) n. comb. (Syn. Schistorchis callyodontis Yamaguti, 1942 ) ( Fig. 11 from Yamaguti 1942; Figs. 1–3 present study).

2b. Genital pore submedian, sinistral; egg ovoid, 45–65 × 25–40.. Plesioschistorchis manteri ( Gupta & Tandon, 1984) n. comb. (Syn. Schistorchis manteri Gupta & Tandon, 1984 ) (Fig. 12).

3a. Genital pore median; ventral sucker located apart from ovary and intestinal bifurcation (latter area crowded by glandular cells); egg 75–81 × 42–50.......................................... Plesioschistorchis sigani ( Yamaguti, 1942) n. comb. (Syn. Schistorchis sigani Yamaguti, 1942 ) ( Fig. 13 ).

3b. Genital pore submedian, sinistral; ventral sucker close to ovary and intestinal bifurcation; egg 69–77 × 40–56........................................................................ Plesioschistorchis haridis ( Nagaty, 1957) n. comb. (Syn. Schistorchis haridis Nagaty, 1957 ) (Fig. 14 from Nagaty 1957; Figs. 4 –6 present study).

a Figure(s) listed in parentheses at the end of each couplet are redrawn from the type description as indicated by the authority for each species. Where more than one authority is given or another reference is used (e.g. re-description of species), the source of the figure(s) is also indicated.

Earlier we had established that S. carneus , S. paruchini , S. skrjabini and S. tetrodontis n. comb. composed Schistorchis sensu stricto, members of which possessed 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-rectangular-shaped 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 infect the intestine of marine Tetraodontiformes . In our current study, we found two of six specimens of the white-spotted puffer, Arothron hispidus (locally known as “Hadroom”) ( Tetraodontiformes : Tetraodontidae ), collected from the Red Sea off southern Hurghada and off Safaga, Egypt, to be infected with Schistorchis carneus , the type species of Schistorchis , and we re-describe this species below.

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 7¯8. Paraschistorchis zancli (Hanson, 1953) n. comb. and Paraschistorchis longivesiculurus (Hafeezullah, 1981) n. comb. 7. P. zancli ventral view of adult redrawn from Hanson (1953, Fig. 2a). 8. P. longivesiculurus ventral view of adult redrawn from Hafeezullah (1981, Fig. 1). Abbreviations: An, Anus; Ce, Cecum; EA, Excretory arm/duct; EP, Excretory pore; Es, Esophagus; EV, Excretory vesicle; GP, Genital pore; MG, Mehlis’ gland; OS, Oral sucker; Ov, Ovary; PC, Prostatic cells; Ph, Pharynx; SR, Seminal receptacle; SV, Seminal vesicle; Te, Testes; Ut, Uterus; VD, Vitelline duct; VF, Vitelline follicles; VR, Vitelline reservoir; VS, Ventral sucker.

FIGURES 9¯10. Paraschistorchis seychellesiensis (Toman, 1989) n. comb. and Paraschistorchis stenosoma (Hanson, 1953) n. comb. 9. P. seychellesiensis ventral view of adult redrawn from Toman (1989, Fig. 2b). 10. P. stenosoma ventral view of adult redrawn from Hanson (1953, Fig. 1a). Abbreviations: An, Anus; Ce, Cecum; EA, Excretory arm/duct; EP, Excretory pore; Es, Esophagus; EV, Excretory vesicle; GP, Genital pore; LC, Laurer’s canal; MG, Mehlis’ gland; OS, Oral sucker; Ov, Ovary; Ph, Pharynx; SR, Seminal receptacle; SV, Seminal vesicle; Te, Testes; Ut, Uterus; VF, Vitelline follicles; 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 13¯14. Plesioschistorchis sigani (Yamaguti, 1942) n. comb. and Plesioschistorchis haridis (Nagaty, 1957) n. comb. 13. P. sigani ventral view of adult redrawn from Yamaguti (1942, Fig. 16). 14. P. haridis ventral view of adult redrawn from Nagaty (1957, Fig. 1). Abbreviations: Ce, Cecum; EA, Excretory arm/duct; EP, Excretory pore; EV, Excretory vesicle; GP, Genital pore; LC, Laurer’s canal; MG, Mehlis’ gland; OD, Ovarian duct; OS, Oral sucker; Ov, Ovary; Ph, Pharynx; PP, Pars prostatica; SR, Seminal receptacle; SV, Seminal vesicle; Te, Testes; Ut, Uterus; VD, Vitelline duct; 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.

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.