Astiotrema reniferum ( Looss, 1898 ) Looss, 1900

Karar, Yasser F. M., Blend, Charles K., Dronen, Norman O. & Adel, Asmaa, 2021, Towards resolving the problematic status of the digenean genus Astiotrema Looss 1900: An updated concept and revision of species composition for Astiotrema (sensu stricto), Zootaxa 4991 (1), pp. 36-72 : 41-44

Astiotrema reniferum ( Looss, 1898) Looss, 1900

( Figs. 1–5 )

(Syns.: Distomum unicum Looss, 1896 nec Molin, 1859; Distomum reniferum Looss, 1898 ; Astia renifera [ Looss, 1898] Looss, 1899; Astiotrema elongatum Mehra, 1931 ; Astiotrema loossii Mehra, 1931 ; Astiotrema gangeticus Harshey, 1932 ; Astiotrema indica Thapar, 1933 ; Astiotrema spinosa Chatterji, 1933 ; Astiotrema rami Bhalerao, 1936 ; Astiotrema dassia Dayal, 1938 ; Astiotrema hoshiarpurium Gupta, 1954 ; Astiotrema thapari Gupta, 1954 ; Astiotrema giganticum Tiwari, 1958 ; Astiotrema lobiorchis Tiwari, 1958 ; Astiotrema lissemysi Qazi & Qazi, 1963 ; Astiotrema longicirra Dwivedi, 1966 ; Astiotrema kachugai Gupta & Jahan, 1978 n. syn.; Astiotrema pseudobagri Wang in Wang, Zhao, Ghen & Tao, 1983 n. comb.; Gauhatiana pseudobagri Wang in Wang, Zhao, Ghen & Tao, 1983 n. syn.; Astiotrema manteri Gupta & Saxena, 1987 n. syn.)

Records (see Table 1 ): 1. Looss (1899); 2. Mehra (1931b); 3. Harshey (1932); 4. Chatterji (1933); 5. Thapar (1933); 6. Bhalerao (1936); 7. Dayal (1938); 8. Gupta (1954); 9. Tiwari (1958); 10. Yeh & Fotedar (1958); 11. Khalil (1959, 1969); 12. Mehrunnisa & Qazi (1963); 13. Agrawal (1966a, 1966b); 14. Dwivedi (1966); 15. Kumari et al. (1972); 16. Cho & Seo (1977); 17. Gupta & Jahan (1978); 18. Wang et al. (1983); 19. Gupta & Saxena (1987); 20. Tawfik et al. (1996); 21. Koiri & Roy (2016).

Remarks: Astiotrema reniferum is the type species of Astiotrema and represents one of the most commonly known and frequently reported species of this genus. Several of these records were identical with the original description of A. reniferum in morphology, host groups, and sharing same or close localities (see Yeh & Fotedar 1958; Khalil 1959, 1969; Agrawal 1966a, 1966b; Kumari et al. 1972; Khalil & Thurston 1973; Cho & Seo 1977) while there were some doubtful or disputed records based on either some critical morphological differences, which caused an overlap with other closely related genera, or an unusual host record (see Bray et al. 2006). Our investigations on these confirmed records of A. reniferum revealed several variations in some morphological features of A. reniferum which were noted either among different publications or in the specimens of the same species collected from the same host (see Yeh & Fotedar 1958; Kumari et al. 1972). These variations include: (i) variable sucker size which ranges from either oral sucker slightly larger or smaller than ventral sucker to equally sized suckers; (ii) change in esophagus length from fairly long to sometimes short or indistinct in contracted specimens; (iii) seminal receptacle shape varied from elliptical, saccular or kidney-shaped as well as variable in size; (iv) variation of posterior extension of cirrus-pouch from a position slightly anterior to ovary to slightly posterior to it; (v) testes shape varied from globular to oval or sometimes irregular as well as their lobulation degree from entire to slightly or deeply lobed; (vi) testes position relative to each other whether tandem, obliquely tandem or rarely oblique; (vii) intestinal ceca terminate near posterior extremity of the body or more anterior to it at about mid-post-testicular area; (viii) vitelline follicles sometimes small aggregations with few follicles or condensed and numerous; (ix) extent of tegument spination from anterior extremity reaching to near level of midbody, covering first two thirds of body or terminating at posterior extremity; (x) differences in location of maximum body width from being in anterior third to around midbody level; (xi) presence or absence of minute esophageal glands; and (xii) vitellarium distribution where the anterior extent of the vitelline fields reaches either the anterior extent of the ovarian level or a little anterior to the level of the ventral sucker, but never reaching the level of the intestinal bifurcation, whereas the posterior extent of vitelline follicles terminates at the level of the posterior margin of the anterior testis or extends to the level of the posterior margin of the posterior testis.

Slight variations observed in size of suckers, maximum body width, testes shape, lobulation degree of testes, posterior extent of intestinal ceca, and the anterior and posterior extent of the vitellarium are greatly affected by host-induced changes, range of geographical distributions and samples sizes used. Concerning differences in seminal receptacle shape and size as well as abundance of vitelline follicles, these can indicate developmental changes which depend on the maturity of the worm. In addition, variation in esophagus length, seminal receptacle position, posterior extent of cirrus-pouch, testes position relative to each other, and tegument spination are influenced by the degree of relaxation of specimens and affected by the different treatments used in parasite preparation, particularly fixation reagents, flattening and staining methods. All these slight variations reflect intraspecific variability and are not indicative of a lack of conspecificity within A. reniferum . Accordingly, we conclude the reliable morphological characteristics of A. reniferum include the following combinations of characters: (i) suckers of roughly equal size, (ii) vitelline field extent ranges from ventral sucker level to the level of the posterior margin of the posterior testis, (iii) ceca extend well into the post-testicular area and terminate near the posterior extremity of the body, (iv) ovary located midway between ventral sucker and anterior testis and (v) the presence of a long esophagus. Therefore, we concur with Yeh & Fotedar (1958) in synonymizing A. dassia , A. elongatum , A. gangeticus , A. hoshiarpurium , A. indica , A. loossii , A. rami , A. spinosa and A. thapari with A. reniferum . In addition, the following synonymies are also included with A. reniferum : A. giganticum , A. lissemysi , A. lobiorchis and A. longicirra (see Siddiqi 1965; Dwivedi & Chauhan 1970; Fotedar 1971; Simha & Chattopadhyaya 1971; Verma 1973; Gupta & Jahan 1978; Gupta & Singh 1985).

Astiotrema kachugai was erected by Gupta & Jahan (1978) for specimens from the intestine of the three-striped roofed turtle, Batagur dhongoka (Gray) (Syn. Kachuga dhongoka Boulenger ) ( Testudines : Geoemydidae ), from Udaipur, Rajasthan, India. Gupta & Jahan (1978) differentiated A. kachugai from all known species of Astiotrema by the absence of a seminal receptacle. They stated that A. kachugai exhibited a great similarity with A. reniferum except for its larger size, presence of esophageal glands, and in the extension of vitelline fields from the level of the anterior margin of the ventral sucker or a little anterior to it to the mid-level of or a little anterior to the posterior testis. Astiotrema is characterized by having a seminal receptacle, but sometimes it can become very difficult to observe when uterine coils overlap and cover it, specimens have not reached full maturity, and/or there is overlap and crowding among the ovary, Mehlis’ gland and anterior testes. Gupta & Jahan (1978, figs. 1–3) seem to have misidentified the structure next or posterior to the ovary, which they considered to be the öotype surrounded by a large number of Mehlis’ gland cells; it appears to be a small seminal receptacle overlapped by several Mehlis’ gland cells. Gupta & Saxena (1987) reported A. manteri from the intestine of the Indian tent turtle, Pangshura tentoria (Gray) (Syn. Kachuga intermedia Boulenger ) ( Testudines : Geoemydidae ), in Lucknow, India. Both A. manteri and A. kachugai share the same host group ( Geoemydidae ) and are identical in all features except esophageal glands which are not reported in A. manteri ( Gupta & Saxena 1987) . The characteristics used in differentiating A. kachugai and A. manteri from A. reniferum fall within the range of intra-specific variation for A. reniferum ; consequently, we conclude both A. kachugai and A. manteri as synonyms of A. reniferum .

Wang et al. (1983) collected G. pseudobagri from the intestine of the yellow catfish, Tachysurus fulvidraco (Richardson) (Syn. Pseudobagrus fulvidraco [Richardson]) ( Siluriformes : Bagridae ), from Hongze Lake, China. Our review pointed out that G. pseudobagri lacks some characteristics of species of Gauhatiana Gupta, 1953 , particularly vitellarium in two distinct clusters in lateral fields on each side of the body and in having an equatorial ovary (see Gupta 1953; Font & Lotz 2008); however, G. pseudobagri has all the characteristics of species of Astiotrema , thereby we believe it to belong in Astiotrema . Indeed, A. pseudobagri n. comb. and A. reniferum are identical in all morphological features except for an indistinct esophagus in A. pseudobagri (see Wang et al. 1983, fig. 4; Note: figs. 3 & 4 in Wang et al. 1983, p. 132 of Allocreadium (Allocreadium) ctenopharyngodonis Wang in Wang, Zhao, Ghen & Tao, 1983 and G. peudobagri are reversed in the figure legend). Several records reported A. reniferum from various fishes; however, the airbreathing catfishes (i.e., species of Clarias Scopoli [ Siluriformes : Clariidae ]) represent the most commonly known fish group harboring A. reniferum ( Yeh & Fotedar 1958; Khalil 1959, 1969; Kumari et al. 1972). Bray et al. (2006) referred to some doubtful or disputed host records for A. reniferum that include two cichlids, the Nile tilapia , Oreochromis niloticus (Linnaeus) , and the blue tilapia , Oreochromis aureus (Steindachner) ( Perciformes : Cichlidae ) ( Tawfik et al. 1996; El Garhy 2003), as well as the fish known locally in Africa as the “semutundu”, Bagrus docmak (Forsskål) ( Perciformes : Bagridae ) ( Khalil & Thurston 1973). Based on having an identical morphology, parasitizing the same fish group ( Siluriformes ) and the wide distribution of A. reniferum from northeast Africa to Asia, A. pseudobagri herein is considered another synonym of A. reniferum .

Kumari et al. (1972) discussed the large amount of intraspecific variation observed in A. reniferum and pointed out that the generic diagnosis of the Indian Pseudoparamacroderoides Gupta & Agarwal, 1968 , was identical to that of Astiotrema except for the position of the ovary, shape of the excretory vesicle and larger spines at the oral sucker than on the body. Kumari et al. (1972) did not believe these variations to be of generic importance and considered Pseudoparamacroderoides congeneric with Astiotrema , believing Pseudoparamacroderoides seenghali Gupta & Agarwal, 1968 and Pseudoparamacroderoides vittatusi Kakaji, 1969 as junior synonyms of A. reniferum . Yamaguti (1971) had earlier established Pseudoparamacroderoides as a subgenus within Paramacroderoides Venard, 1941 based on similar morphology, hosts and localities among constituent species. Agarwal & Kumar (1983) recognized neither the synonymies of Yamaguti (1971) nor Kumari et al. (1972) and established another species, Pseudoparamacroderoides raychaudhurii Agarwal & Kumar, 1983 , while Agarwal & Agarwal (1985) followed with a fourth species, Pseudoparamacroderoides keni Agarwal & Agarwal, 1985 . Font & Lotz (2008) continued the synonymy of Pseudoparamacroderoides and its representative species within Paramacroderoides . Investigations by Tkach et al. (2010) revealed that Indian members of Paramacroderoides (Syn. Pseudoparamacroderoides ) differ substantially from North American members of Paramacroderoides in both morphology and host-parasite data, therefore, they synonymized Pseudoparamacroderoides with Macroderoides Pearse, 1924 —the morphologically most similar genus—and suggested the possibility of further change in the systematic position of members of Pseudoparamacroderoides with future molecular analysis. Whether Pseudoparamacroderoides represents a distinct genus or is synonymous with either Macroderoides or Paramacroderoides , representative species of these three genera can be distinguished clearly from members of Astiotrema by having a bipartite seminal vesicle and an I-shaped excretory vesicle (see Font & Lotz 2008).

Figures

FIGURES 1–5. Astiotrema reniferum (Looss, 1898) Looss, 1900 revealing some intra-specific variations in esophagus extension, vitellarium distribution and maturation, testes configuration, and ovary shape. 1. A. reniferum (Syn. Distomum unicum Looss, 1896 nec Molin, 1859), ventral view, redrawn from Looss (1896, fig. 20). 2. A. reniferum (Syn. Astiotrema giganticum Tiwari, 1958), dorsal view, redrawn from Tiwari (1958, fig. 1). 3. A. reniferum (Syn. Astiotrema thapari Gupta, 1954), ventral view, redrawn from Gupta (1954, fig. 4). 4. A. reniferum (Syn. Astiotrema loossii Mehra, 1931), dorsal view, redrawn from Mehra (1931b, p. 187). 5. A. reniferum (Syn. A. loossii), ventral view, redrawn from Dwivedi (1966, fig. 2). Abbreviations: AT, anterior testis; Ce, cecum; CP, cirrus-pouch; Eg, eggs; EP, excretory pore; Es, esophagus; EV, excretory vesicle; GP, genital pore; LC, Laurel’s canal; Oo, oötype; OS, oral sucker; Ov, ovary; Ph, pharynx; PP, pars prostatica; PT, posterior testis; SR, seminal receptacle; SV, seminal vesicle; Ut, uterus; VD, vitelline duct; V-D, vas-deferens; VF, vitelline follicle; VS, ventral sucker. Scale bars: Fig. 1 = 1,000 µm; Fig. 2 = 2,000 µm; Fig. 3 =2,000 µm; Fig. 4 = 500 µm; Fig. 5 = 1,000 µm.