Heterorchis Baylis, 1915

Curran, Stephen S., Dutton, Haley R., Warren, Micah B., Preez, Louis du & Bullard, Stephen A., 2021, Two new species of Cephalogonimidae Looss, 1899 (Digenea: Plagiorchioidea) from Africa (Mozambique and Guinea), including a new phylogenetic hypothesis for related plagiorchioids, International Journal for Parasitology: Parasites and Wildlife 14, pp. 228-240 : 234-235

3.3. Genus Heterorchis Baylis, 1915

Heterorchis cf. crumenifer Baylis, 1915

3.3.1. Description ( Figs. 6 and 7 )

[Based on 12 mature specimens] Body oval, 1600–2900 long, 580–1125 wide near midbody. Tegument and suckers entirely covered by robust scale-like spines. Oral sucker subglobular, subterminal, 125–250 long, 173–300 wide. Prepharynx, very short, 18–50 long (seven measured), surrounded by muscular, lip-like rim emerging from anterior margin of pharynx. Pharynx dolioform, 78–135 long, 88–130 wide, surrounded by gland cells. Oesophagus present, longer than prepharynx, 18–85 long. Ventral sucker nearly circular, 290–470 long, 268–490 wide. Oral to ventral sucker width ratio 1:1.5–1.8 (10 specimens). Forebody 320–720 long, or 20–26% of body length. Intestine bifurcating at level about midway between suckers, caeca blind, extending to near posterior region of hindbody. Postcaecal space 125–260 long or 6–11% of body length.

Testes elongate, opposite, intercaecal in middle of hindbody; right testis 420–710 long, 130–210 wide, left testis 320–700 long, 120–190 wide; right testis longer than left testis (n = 7), wider than left testis (n = 9), usually extending more posteriorly than left testis (90%, n = 39). Post-testicular space 400–850 or 21–33% of body length. Cirrus sac with anterior end curving sharply toward left side, extending posterior past ventral sucker, 500–1000 long, 110–140 wide, containing bipartite seminal vesicle, pars prostatica, and elongated bending or coiling cirrus. Proximal portion of seminal vesicle always larger than distal portion; proximal portion 188–245 long, 68–105 wide; distal portion 78–135 long, 55–80 wide. Prostatic bulb longer than wide, 65–133 long, 28–125 wide. Cirrus 280–360 long, 23–45 wide, extruded in two specimens; extruded cirrus with irregular surface, possibly caused by minute spines. Cirrus sac emptying into elongated tubular genital atrium on left side; genital atrium submarginal, 50–133 long, 28–63 wide. Genital pore slightly submarginal, opening on left side at level of intestinal bifurcation.

Ovary, distinctly 4–7 lobed, elongate, submedian on right side, immediately anterior to and usually contiguous with right testis, 235–480 long, 125–250 wide. Seminal receptacle usually overlapping or immediately adjacent to left edge of ovary, with posterior margin extending slightly more posterior than ovary, subspherical, 93–155 long, 90–133 wide (n = 5), or transverse elongated, 88–135 long, 58–83 wide (n = 3). Ootype and Mehlis’ gland immediately adjacent and median to anterior half of ovary. Laurer’ s canal not observed. Vitellarium comprised of two lateral groups of irregularly shaped follicles; follicles extra-caecal and surrounding caeca, extending from mid-level of ventral sucker to a level approximately 2/3 of body length from the anterior end. Vitelline reservoir median, triangular to digitiform, 38–88 long, 15–50 wide (seven measured), communicating with oviduct. Uterus occupying most of ventral hindbody. Proximal uterus descends from ootype in dorsal hindbody toward the posterior end, with coils

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expanding in posterior hindbody prior to ascending in ventral hindbody and communicating with prominent, highly muscular metraterm. Metraterm surrounded by gland cells, situated immediately adjacent to cirrus sac and following contour of cirrus on left side; proximal portion 175–400 long, 25–50 wide, surrounded by thin layer of gland cells (10 measured, width measurement not including gland cells); distal portion 200–400 long, 30–90 wide (nine measured, width measurement not including gland cells); entire metraterm 375–725 long (nine measured). Eggs filling uterus, operculated, 20–30 long, 10–15 wide (28 measured from distal region of uterus near junction of metraterm).

Excretory bladder Y-shaped, main stem an enormous tear-shaped swollen bladder occupying much of dorsal hindbody, extending anteriorly into ovarian level. Main collecting ducts immediately swelling near junction with main stem, forming oval to elongate bladders, 125–415 long, 38–75 wide (seven measured); bladders reverting to narrow main collection ducts 15–25 in diameter, extending anteriorly and laterally in forebody to level of oesophagus then descending posteriorly in lateral forebody. Excretory pore, dorsal, comprising an enormous dorsal circular opening, 210–510 long, 210–620 wide. Posterior margin of dorsal opening at 220–575 from posterior end or 13–19% of body length.

Type host: marbled lungfish, Protopterus aethiopicus Heckel, 1851 , (Lepidosireniformes: Protopteridae ).

Other hosts: West African lungfish, Protopterus annectens (Owen, 1839) ( Dollfus, 1929, 1950; present study).

Site in host: intestine.

Prevalence: Eighty-four worms were collected from four of six fish examined; mean intensity = 21 +/ 19 (standard deviation).

Type locality: Lake Victoria , Uganda .

Other localities: Maroua, Cameroon ( Dollfus, 1929); Ogooue´River, Democratic Republic of the Congo ( Dollfus, 1950); Karingani Game Reserve, Mozambique (present study).

Specimens deposited: 10 voucher specimens (USNM 1642462- 1642471).

Sequence deposited: GenBank No. MW586924.

3.3.2. Remarks

The unique condition of the excretory system of these worms allowed us to easily identify them as belonging in the enigmatic genus Heterorchis . Thus far, four species, all from Africa, have been described in the genus. Heterorchis crumenifer (type species) was originally described infecting the intestine of a specimen of P. aethiopicus collected from Ugandan waters of Lake Victoria ( Baylis, 1915). Dollfus (1950) reported H. crumenifer infecting the intestine of P. annectens from Democratic Republic of the Congo and provided a description for two specimens in his collection. Dollfus (1929) discovered juvenile forms of a worm that he described as Distoma protopteri Dollfus, 1929 infecting the intestine of P. annectens collected at Maroua, Cameroon. Dollfus (1950) later considered these forms to represent a synonym of H. crumenifer , but it should be noted that this identification (based on immature traits) must be considered tentative. Our material and adult material studied by Baylis (1915) and Dollfus (1950) compare favorably except that Baylis (1915) reported egg size of 40 μm by 20 μm, which is substantially larger than eggs we observed (20–30 by 10–15 μm) and sizes reported by Dollfus (1950), (28–31 by 15–16 μm). Baylis (1915) deposited the original type material for H. crumenifer in the Natural History Museum, London, UK, but we were not able to access the museum during preparation of the manuscript in 2019–20 to confirm the egg size in specimens. The present identity of our material should therefore remain tentative as ( Heterorchis cf. crumenifer ), until a thorough comparison with the type material can be made and egg sizes from the type material can be confirmed. Three other species have been described in Heterorchis since its erection.

Heterorchis protopteri Thomas, 1958 was described from the intestine of P. annectens collected from the Volta River, Ghana. Thomas (1958b) fixed his specimens using “slight coverslip pressure” and differentiated his specimens from H. crumenifer by them having a fully marginal genital pore, relatively larger ventral sucker (oral to ventral sucker width ratio of 1:1.8) compared with 1:1.5 ( Baylis, 1915), 1:1.4–1.6 ( Dollfus, 1950) and 1.1.5–1.8 (present study), posterior margin of testes being pointed rather than more rounded, slightly more posterior seminal receptacle, and egg size. Except for egg size, we think the differences of specimens described by Thomas (1958b) can all be produced by adding pressure. We could not identify any useful features for differentiating H. protopteri from H. crumenifer . Consequently, we consider H. protopteri a species inquirenda.

Heterorchis ghanensis Fischthal & Thomas, 1968 was described based on a single specimen infecting the intestine of a frog ( Hyperolius nitidulus Peters ) collected from Accra, Ghana. Fischthal and Thomas (1968) believed that this specimen differed from H. crumenifer and H. protopteri because they observed a connection between the caeca and excretory bladder. This remarkable feature needs confirmation. Otherwise, we find the description overlaps that of H. crumenifer . We consider H. ghanensis a species inquirenda.

Heterorchis senegalensis Vassiliad`es & Richard, 1970 was described infecting the intestine of P. annectens from Dakar, Senegal. Vassiliad`es and Richard (1970) described this species based on well-fixed specimens lacking pressure and considered it to differ from the three other named species based on testis shape and testis size and placed emphasis on the left testis being the more posterior one vs it being the more anterior one in the three previously named species. We observed the left testis extending more posteriorly than the right one in 10% of the specimens of H. cf. crumenifer we collected. While this trait is therefore not effective for differentiating species of Heterorchis , we do consider H. senegalensis distinguishable from H. crumenifer on the basis that the caecal extent is further posterior in H. crumenifer (to near the posterior end of the body or 6–11% of body length) compared with slightly beyond the posterior margin of posterior testis or ~21% of body length in H. senegalensis ( Baylis, 1915; Dollfus, 1950; Vassiliad`es and Richard, 1970).

Figures

Fig. 6. Ventral view of Heterorchis cf. crumenifer from the intestine of the West African lungfish, Protopterus annectens (Owen). Abbreviations: caecum, c; cirrus, ci; cirrus sac, cs; dorsal opening to excretory bladder, do; distal portion of seminal vesicle, ds; distal uterus, du; excretory bladder, eb; excretory duct, ed; genital atrium, ga; genital pore, gp; left testis, lt; metraterm, m; ootype, oo; ovary, ov; pars prostatica, pp; proximal portion of seminal vesicle, ps; proximal uterus, pu; right testis, rt; seminal receptacle, sr; vitelline follicle, vf; vitelline reservoir, vr.

Fig. 7. Dorsal view of excretory system of Heterorchis cf. crumenifer from intestine of the West African lungfish, Protopterus annectens (Owen). Abbreviations: cd; collection ducts, ep; excretory pore, ms; main stem of excretory bladder, ob; oval or elongated bladders, os; oral sucker, vs; ventral sucker.