Orientocreadium batrachoides Tubangui, 1931

Karar, Yasser F. M., Blend, Charles K., Dronen, Norman O. & Adel, Asmaa, 2023, Towards resolving the problematic status of the digenean genus Astiotrema Looss 1900: Taxa excluded from Astiotrema (sensu stricto) with special reference to plagiorchioid genera closely related to the restricted concept of Astiotrema, Zootaxa 5284 (3), pp. 445-495 : 464-467

Orientocreadium batrachoides Tubangui, 1931

( Fig. 18 )

(Syns. Neoganada barabankiae Dayal, 1938 ; Ganadotrema indica Dayal, 1949 ; Neoganada secunda Dayal, 1949 ; Ganadotrema mahendrai Gupta, 1951 ; Ganadotrema phillipai Gupta, 1951 ; Ganadotrema vermai Gupta, 1951 ; Orientocreadium dayalai Saksena, 1958 ; Orientocreadium dayali Yamaguti, 1958 ; Orientocreadium indica ( Dayal, 1949) Saksena, 1958 ; Orientocreadium mahendrai [ Gupta, 1951] Saksena, 1958; Orientocreadium philippai [ Gupta, 1951] Saksena, 1958; Orientocreadium raipurensis Saksena, 1958 ; Orientocreadium vermai [ Gupta, 1951] Saksena, 1958; Orientocreadium bharati Saksena, 1960 ; Orientocreadium umadasi Saksena, 1960 ; Orientocreadium lazeri Khalil, 1961 ; Orientocreadium barabankiae [Dayal, 1938] Beverley-Burton, 1962; Orientocreadium secundum [ Dayal, 1949] Beverley-Burton, 1962; Ganada barabankiae [Dayal, 1938] Fischthal & Kuntz, 1963; Ganada indica [ Dayal, 1949] Fischthal & Kuntz, 1963; Astiotrema gangesense nom. nov.; Astiotrema gangeticus Gupta & Singh, 1985 nec Harshey, 1932 n. syn.)

Records. 1. Tubangui (1931); 2. Dayal (1938a, 1949); 3. Tubangui & Masiluñgan (1944); 4. Gupta (1951); 5. Saksena (1958, 1960); 6. Khalil (1961); 7. Beverley-Burton (1962); 8. Agrawal (1963, 1964); 9. Fischthal & Kuntz (1963); 10. Kakaji (1969); 11. Zaidi & Khan (1977); 12. El-Naffar et al. (1984); 13. Sirikantayakul (1985); 14. Bhadauria & Dandotia (1988); 15. Hafeezullah (1989); 16. Moravec & Sey (1989); 17. Dutta (1995); 18. Hafeezullah & Dutta (1999); 19. Gibson et al. (2005); 20. Taeleb & Lashein (2013); 21. Tepe et al. (2013); 22. Vankara et al. (2014); 23. Zhokhov et al. (2017); 24. Al-Moussawi et al. (2018); 25. Dumbo et al. (2019).

Remarks. Astiotrema gangeticus was described by Gupta & Singh (1985) for specimens collected from the intestine of the Philippine catfish, Clarias batrachus (Linnaeus) ( Siluriformes : Clariidae ), from the River Ganges, Kanpur, India. Gupta & Singh (1985) apparently were not aware that their proposed name “ Astiotrema gangeticus ” was pre-occupied (i.e., Astiotrema gangeticus Harshey, 1932 ) for specimens earlier gathered from the intestine of the flap-shelled turtle, Emyda granosa Strauch ( Testudines : Trionychidae ), in Allahabad, India ( Harshey 1932); specimens of Harshey (1932) are currently considered a synonym of A. reniferum (see Yeh & Fotedar 1958; Karar et al. 2021; WoRMS 2022b). Based on (i) distinctive morphology and different host-parasite data (particularly host type, feeding habits and habitats) of specimens collected by Gupta & Singh (1985) vs those of Harshey (1932) and (ii) according to the Principle of Priority by the ICZN as well as (iii) our desire to correct a homonym, we rename the specimens of Gupta & Singh (1985) Astiotrema gangesense nom. nov.; the species designation refers here to the fish locality “River Ganges” where worms were recorded.

Gupta & Singh (1985) distinguished their specimens from other taxa of Astiotrema by some disputed, variable, overlapping and/or unspecialized features including (i) the difference in esophagus length, posterior extent of cirrus-pouch relative to ovary, distribution of body spines and body size; (ii) slight variations in the anterior extent of vitellarium and genital pore position (whether at bifurcal level or immediately post-bifurcal compared to some taxa of Astiotrema ); and (iii) they relied on a problematic taxonomic feature for differentiating among taxa of Astiotrema , the absence of the seminal receptacle (the diagnosis of Astiotrema indicates the presence of either a large or small canalicular, post-ovarian seminal receptacle with few spermatozoa or overlapped by uterine coils - see Yeh & Fotedar 1958; Pojmańska et al. 2008; Karar et al. 2021). In addition, the presence or absence of the seminal receptacle represents a strong diagnostic feature for differentiating at the genus and subfamily levels, not for the species-level only as we have experienced. Thus, these previous reasons make the comparison by Gupta & Singh (1985) inadequate to distinguish their material as a distinct species from other representatives of Astiotrema . However, we note two features we find unique for A. gangesense compared to taxa of Astiotrema (sensu lato): (i) vitelline fields confluent in posterior half of post-testicular space forming a U-shaped posterior extent; and (ii) the male genital system (see Gupta & Singh 1985, fig. 1A) has what appears to be an external vesicular seminal vesicle, confined in the space between the cirrus-pouch and ovary; not a seminal receptacle overlapping the anterior margin of the ovary as stated in the main text, since the seminal receptacle in Astiotrema generally is positioned posterior/postero-lateral to the ovary, not anterior to it, and distinctly separated from the cirrus-pouch (see Yeh & Fotedar 1958; Pojmańska et al. 2008; Karar et al. 2021). Consequently, we believe Gupta & Singh (1985) misidentified their specimens as Astiotrema . These specimens are plagiorchioids belonging to the Orientocreadiidae as members of the only and type-genus, Orientocreadium , based on the combined following characteristics: parasitizing intestine of freshwater fish; mouth close to anterior extremity, opens in oral sucker; hermaphroditic duct and sac absent; excretory vesicle Y-shaped with terminal excretory pore at posterior extremity; suckers and pharynx present; testes post-ovarian; cirrus-pouch present; intestinal ceca two; vitellarium follicular, extensive; elongate to fusiform, aspinose body; genital pore in forebody, median, post-bifurcal; oral sucker lacks lateral muscular papillae or lappets; much of uterus reaches into post-testicular region; external seminal vesicle present; and prepharynx distinct (see Bray 2008f).

Our survey of digeneans parasitizing the intestine of the Philippine catfish, C. batrachus , and its synonyms referred to several records that included three representatives of Orientocreadium : (i) Orientocreadium batrachoides Tubangui, 1931 ( Tubangui 1931; Dayal 1938a; Tubangui & Masiluñgan 1944; Gupta 1951; Saksena 1958, 1960; Bhadauria & Dandotia 1988; Hafeezullah 1989; Hafeezullah & Dutta 1999; Taeleb & Lashein 2013; Tepe et al. 2013; Vankara et al. 2014); (ii) Orientocreadium clariae ( Chatterji, 1933) Yamaguti, 1954 (see Chatterji 1933); and (iii) Orientocreadium lucknowensis Nigam, Chandra, Johri & Saxena, 2015 ( Nigam et al. 2015). Orientocreadium clariae and O. lucknowensis are extremely similar to O. batrachoides except O. clariae has smaller eggs (18 × 12 μm in O. clariae vs ≥ 25 × 18 μm in O. batrachoides ) (see Beverley-Burton 1962) and O. lucknowensis is characterized by the presence of a small seminal receptacle overlapping the ovary (cf. canalicular seminal receptacle) as stated by Nigam et al. (2015, fig. 1.1); this contradicts the diagnosis of members of the Orientocreadiidae which indicates all have a uterine seminal receptacle (see Jones & Bray 2008). Accordingly, we consider O. lucknowensis as incertae sedis until the true nature of the small, saccular structure overlapping the ovary can be confirmed.

Regarding geographical distribution, O. batrachoides exhibits a wide distribution in freshwater fishes within various localities of both Africa and Asia: China ( Gibson et al. 2005); Egypt ( Fischthal & Kuntz 1963; El-Naffar et al. 1984; Taeleb & Lashein 2013); Ethiopia ( Zhokhov et al. 2017); India ( Dayal 1938a, 1949; Gupta 1951; Saksena 1958, 1960; Agrawal 1963, 1964; Kakaji 1969; Bhadauria & Dandotia 1988; Hafeezullah 1989; Dutta 1995; Hafeezullah & Dutta 1999; Vankara et al. 2014); Iraq ( Al-Moussawi et al. 2018); Mozambique ( Dumbo et al. 2019); Pakistan ( Zaidi & Khan 1977); Philippines ( Tubangui 1931; Tubangui & Masiluñgan 1944; Sirikantayakul 1985); Sudan ( Khalil 1961); Turkey ( Tepe et al. 2013); Vietnam ( Moravec & Sey 1989); Zambia ( Beverley-Burton 1962); and Zimbabwe ( Beverley-Burton 1962). Based on the identical morphology of A. gangesense with O. batrachoides , particularly the absence of a canalicular seminal receptacle, approximately the same egg size (28–33 × 13–19 μm), and sharing close localities from the reported geographical area ( India) and from the same host ( C. batrachus ), we find A. gangesense to represent another synonym of O. batrachoides .

Figures

FIGURES 17 & 18. Neoastiotrema trituri (Grabda, 1959) Tkach, 2008 and Orientocreadium batrachoides Tubangui, 1931. 17. N. trituri (syn. Astiotrema trituri Grabda 1959), ventral view, redrawn from Grabda (1959, fig. 1). 18. O. batrachoides (syn. Astiotrema gangeticus Gupta & Singh, 1985 nec Harshey, 1932), ventral view, redrawn from Gupta & Singh (1985, fig. 1A). Abbreviations: AT, anterior testis; Ce, cecum; CP, cirrus-pouch; Eg, egg; EP, excretory pore; Es, esophagus; ESV, external seminal vesicle; EV, excretory vesicle; GA, genital atrium; GP, genital pore; ISV, internal seminal vesicle; Me, metraterm; OC, ôtype complex; OS, oral sucker; Ov, ovary; Ph, pharynx; Pr.Ph, prepharynx; PP, pars prostatica; PT, posterior testis; SR, seminal receptacle; SV, seminal vesicle; Ut, uterus; VF, vitelline follicle; VS, ventral sucker. Scale bars: Fig. 17 = 500 µm; Fig. 18 = 500 µm.