Astiotrema odhneri Bhalerao, 1936

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 : 52-55

Astiotrema odhneri Bhalerao, 1936

( Figs. 17–20 )

(Syns.: Astiotrema reniferum of Odhner, 1911 nec Looss, 1898; Astiotrema orientale Yamaguti, 1937 ; Astiotrema amydae Ogawa, 1938 ; Astiotrema fukuii Ogawa, 1938 ; Astiotrema foochowensis Tang, 1941 ; Astiotrema matthaii Gupta, 1954 ; Astiotrema nathi Gupta, 1954 ; Astiotrema srivastavai Gupta, 1954 ; Astiotrema geomydia Siddiqui, 1958 n. syn.; Astiotrema mehrai Tiwari, 1958 ; Astiotrema sudanensis Khalil, 1959 n. syn.; Astiotrema cirricurvatus Simha & Chattopadhyaya, 1971 n. syn.; Astiotrema brevicaecum Wang, 1987 n. syn.; Astiotrema hanumantharai Dhanumkumari, 1999 n. syn.)

Records (see Table 1 ): 1. Odhner (1911); 2. Bhalerao (1936); 3. Yamaguti (1937); 4. Ogawa (1938); 5. Tang (1941); 6. Gupta (1954); 7. Siddiqui (1958); 8. Tiwari (1958); 9. Yeh & Fotedar (1958); 10. Khalil (1959); 11. Ahluwalia (1960); 12. Dollfus & Simha (1964); 13. Agrawal (1966a); 14. Fotedar (1971); 15. Simha & Chattopadhyaya (1971); 16. Cho & Seo (1977); 17. Wang (1987); 18. Dhanumkumari (1999); 19. Besprozvannykh et al. (2015).

Remarks: Odhner (1911) identified specimens of Astiotrema collected from the intestine of the African or Nile softshell turtle, T. triunguis ( Testudines : Trionychidae ), as A. reniferum . Bhalerao (1936) discussed the specimens of Odhner (1911) and disputed their identity as A. reniferum . This was based on these specimens having (i) shorter ceca terminating at the posterior limit of the posterior testis level, (ii) lobed and differently-shaped testes, (iii) an ovary positioned more anteriorly in the anterior third of the body and (iv) vitellarium distributed differently when compared with the first description of A. reniferum (as Distomum reniferum ) by Looss (1898) and its updates ( Looss 1899, 1900). Therefore, A. odhneri was proposed by Bhalerao (1936) for the specimens of Odhner (1911). Yeh & Fotedar (1958) presented a major revision of 21 species of Astiotrema in which they recognized A. odhneri , synonymized 8 species with it and explained the importance of ceca length as a taxonomic character in Astiotrema . Khalil (1959) synonymized A. odhneri with A. reniferum based on (i) the variability in the length of ceca (i.e., terminations of ceca range from near the posterior extremity to the posterior margin of the posterior testis) in specimens collected from the Sudan from the type host of A. odhneri and (ii) the nonspecific importance of testis shape and lobulation as explained by Yeh & Fotedar (1958). Fotedar (1971) disagreed with the action by Khalil (1959); pointing out the consistent difference in cecal length between the two species as well as the possibility that Khalil (1959) had dealt with two different species of Astiotrema from the same host. At present, the taxonomic status of A. odhneri relative to A. reniferum remains disputed; some authors have accepted their conspecificity (see Khalil 1959; Dollfus & Simha 1964; Siddiqi 1965; Agrawal 1966a; Simha & Chattopadhyaya 1971; El-Naffer et al. 1984; Gupta & Saxena 1987) and others have not (see Yeh & Fotedar 1958; Cho & Seo 1977; Dhar 1977; Besprozvannykh et al. 2015).

Through a detailed review focusing on A. odhneri and A. reniferum , their synonyms and closely related congeners, we found (i) no report, record, comment, description or illustration documenting a noticeably wide variation in the posterior extent of the ceca for a species of Astiotrema ; (ii) the original description of A. reniferum (see Looss 1899) and the revisions by Yeh & Fotedar (1958) and Kumari et al. (1972) clarified that the ceca of A. reniferum terminate either a little anterior to the posterior extremity or midway between the posterior testis and posterior extremity; (iii) based on the specimens of Odhner (1911), subsequent studies of A. odhneri ( Cho & Seo 1977; Besprozvannykh et al. 2015) and the corresponding synonyms for this species made by Yeh & Fotedar (1958), we clarify that in A. odhneri the ceca reliably terminate at the posterior border of the posterior testis; (iv) considering the total change in the posterior extent of the ceca from the level of the posterior extent of the posterior testis to the posterior extremity of the body as a predictable slight variation, this causes overlap among several species of Astiotrema , thus, complicating the taxonomic status of this digenean genus more than it is now. Accordingly, we concur with Yeh & Fotedar (1958) and Fotedar (1971) and consider A. odhneri a species separated from A. reniferum and we support the opinion of Fotedar (1971) that Khalil (1959) dealt with two species of Astiotrema from the same host; the same case observed later by Cho & Seo (1977) who redescribed both A. reniferum and A. odhneri from the intestine of the same host (the Chinese soft-shelled turtle, Pelodiscus sinensis Wiegmann [Syn. Amyda sinensis Stejneger ] [ Testudines : Trionychidae ], from South Korea).

Variation reported in some morphological features of A. odhneri is similar to that observed for A. reniferum : (i) size of oral sucker either slightly larger or smaller than ventral one or suckers equally-sized; (ii) seminal receptacle can vary in shape and size; (iii) posterior extent of cirrus-pouch ranges from a slight distance anterior to ovary to slightly posterior to it; (iv) testes shape and position vary from globular to oval to irregular and from oblique to obliquely tandem; (v) ceca terminate in range from anterior to posterior margins of posterior testis; (vi) spines on tegument extend from anterior extremity to either the anterior limit of last 1/3 of body or to posterior extremity; and (vii) vitelline field distribution, extending either from anterior to ovarian level or level of anterior margin of ventral sucker to either level of anterior margin of posterior testis or posterior margin of it. We think that these variations are neither diagnostic for differentiating species nor cast doubt on conspecificity with A. odhneri . Thus, we concur with Yeh & Fotedar (1958) and consider A. amydae , A. foochowensis , A. fukuii , A. matthaii , A. nathi , A. orientale and A. srivastavai synonyms of A. odhneri .

Siddiqui (1958) described A. geomydia from the intestine of the spiny turtle, Heosemys spinosa (Gray) (Syn. Geomyda spinosa Gray ) ( Testudines : Geoemydidae ), from Aligarh, India, and noted the close resemblance of his specimens with those of A. rami (= A. reniferum —see above), yet recognized both species. Ahluwalia (1960) and Fotedar (1971) considered A. geomydia a synonym of A. impletum . In the current study, A. geomydia is differentiated from A. reniferum by its large post-testicular region and ceca that end near the level of the posterior testis; A. geomydia is differentiated from A. impletum by the shorter anterior extent of its vitellarium (i.e., entirely post-acetabular and extends to level of cirrus-pouch) and ovary being closer to the anterior testis than the ventral sucker. Consequently, we find that A. geomydia neither resembles A. reniferum nor A. impletum and we consider it another synonym of A. odhneri based on its identical morphology and consistent nature of the habits and habitats of the host species (i.e., Testudines ).

Tiwari (1958) described A. mehrai from the intestine of the three-striped or dhond roofed turtle, B. dhongoka ( Testudines : Geoemydidae ), from Raipur, India. Astiotrema mehrai exhibited a close relation with A. reniferum (Syns. A. dassia , A. indica and A. thapari ) based on having equally sized suckers but differed by its possession of rounded testes, shorter ceca and in the distribution of vitelline follicles. Dollfus & Simha (1964) identified specimens of A. reniferum from the intestine of the red-crowned or painted roofed turtle, Batagur kachuga (Gray) (Syn. Kachuga kachuga Smith ) ( Testudines : Geoemydidae ), from Hyderabad, India; this identification was found to be unjustified and the true species should be A. odhneri based on the ceca terminating at the anterior limit of the posterior testis level as well as the presence of a large post-cecal area. Agrawal (1966a) and Simha & Chattopadhyaya (1971) indicated the high spectrum apparent in regard to shape of testes, length of ceca and vitellarium extent, thereby they synonymized A. mehrai with A. reniferum and Gupta & Singh (1985) followed this synonymy; however, A. mehrai differs from A. reniferum by the former possessing ceca that end at the level of the posterior testis and a longer post-cecal area, features typically characteristic of A. odhneri . Due to additional similarities between A. mehrai and A. odhneri (i.e., known geographical distribution [ India] for A. odhneri , main host group [ Testudines ] and morphological variation), we support the view of Fotedar (1971) that A. mehrai is a synonym of A. odhneri .

Khalil (1959) added A. sudanensis from the intestine of the African or Nile softshell turtle, T. triunguis ( Testudines : Trionychidae ), from Sudan and pointed out its resemblance to A. reniferum , but noted that it differed in the relative sizes of the two suckers, the extent of the vitellarium and the smaller size of the eggs. Agrawal (1966a) considered A. sudanensis a synonym of A. reniferum , while Fotedar (1971) cast doubt on the validity of A. sudanensis , clarified its close relationship with A. impletum , and pointed out the necessity of re-examining the specimens of Khalil (1959) to determine the validity of A. sudanensis . Focusing on the type description of A. sudanensis , we did not find any differences between A. sudanensis and A. odhneri . Both species have the same morphology, reported host group ( Trionychidae ) and type host, T. triunguis . Accordingly, we consider A. sudanensis a synonym of A. odhneri .

Astiotrema cirricurvatus was recorded from the intestine of the Nagpur soft-shelled turtle, Nilssonia leithii (Gray) (Syn. Trionyx leithi Alderton ) ( Testudines : Trionychidae ), found in the Manjara (= Manjira) River, Karnataka (previously Mysore) State, India ( Simha & Chattopadhyaya 1971). They differentiated A. cirricurvatus from all other congeneric species by its larger cirrus-pouch, the terminal portion of which curves around the posterior and right lateral border of the ventral sucker. We have observed that several species of Astiotrema have a large cirrus-pouch (see Siddiqui 1958; Wang 1987; Dhanumkumari 1999) while others have a cirrus-pouch of varying sizes. It is also possible that the size of the cirrus-pouch may be influenced by the volume of spermatozoa within it. Concerning the curvature of the terminal portion of the cirrus-pouch (ejaculatory duct) around the posterior and right lateral border of the ventral sucker, this character is present in several species of Astiotrema (see Fischthal & Kuntz 1965; Dhanumkumari 1999; A. impletum from present study). Consequently, we do not think that the size and course of the cirrus-pouch, as the purported characters used by Simha & Chattopadhyaya (1971) for differentiating A. cirricurvatus , are valid, and we consider A. cirricurvatus a synonym of A. odhneri based on their morphological and ecological similarity (i.e., hosts belong to the Trionychidae Fitzinger ).

Wang (1987) described A. brevicaecum from two specimens obtained from the intestine of the Chinese softshelled turtle, Pelodiscus sinensis (Syn. Trionyx sinensis Strauch ) ( Testudines : Trionychidae ), collected in Taining County, Fujian Province, China, and clarified its close relation with A. monticellii . The present study revealed that A. brevicaecum has the same morphological characteristics of A. odhneri as well as the same host family ( Trionychidae ) and is from a previously well-known geographical locality (Asia) for A. odhneri (Syn. A. foochowensis ) (see Tang 1941; Wang 1987). Accordingly, we synonymize A. brevicaecum with A. odhneri .

Dhanumkumari (1999, p. 204) proposed A. hanumantharai for specimens collected from the intestine of two distinctly separate hosts: a freshwater host, the stinging catfish, Heteropneustes fossilis (Bloch) ( Siluriformes : Heteropneustidae ), and a turtle of either a suspicious habitat (i.e., “freshwater”) or a suspicious name (i.e., “ Chelone mydas ” Boulenger [ Testudines : Cheloniidae ]), the green sea turtle, both “from in and around” Visakhapatnam, Andhra Pradesh, India. Astiotrema hanumantharai exhibits a close relationship morphologically with A. reniferum and its synonyms, A. manteri and A. kachugai , as well as a great resemblance to A. odhneri (see Simha & Chattopadhyaya 1971; Syn. A. cirricurvatus ) with just a minor difference that A. hanumantharai has a smaller cirrus-pouch; we thereby conclude A. hanumantharai as a synonym of A. odhneri . The finding by Dhanumkumari (1999) of A. odhneri is the first time this species has been recorded from a freshwater fish. Regarding the suspicious habitat of the reported turtle, Dhanumkumari (1999) stated that Chelonia mydas (Linnaeus) (Syn. Chelone mydas ) ( Testudines : Cheloniidae ) was another host for his specimens despite the fact that C. mydas is distinctly a marine species commonly known as the green sea turtle, green turtle, black sea turtle or Pacific green turtle ( Uetz et al. 2021). Although it does feed at times in freshwater habitats (see Cammarata & Dronen 2020), we suspect that Dhanumkumari (1999) may have been mistaken in determining the exact habitat of C. mydas to be marine, not freshwater. Assuming that the habitat sampled was freshwater, we suspect that Dhanumkumari (1999) may have been mistaken in the identification of the turtle host based on the fact that Visakhapatnam is a city rich in tortoises and freshwater turtles as well as marine ones, and previously recorded hosts of Astiotrema have been limited to freshwater or terrestrial habitats. Accordingly, confirmation is needed for the turtle species sampled.

Figures

FIGURES 17–20. Intra-specific variations observed in Astiotrema odhneri Bhalerao, 1936. 17. A. odhneri (Syn. Astiotrema reniferum of Odhner, 1911 nec Looss, 1898), ventral view, redrawn from Yeh & Fotedar (1958, fig. 5) after Odhner (1911). 18. A. odhneri (Syn. Astiotrema hanumantharai Dhanumkumari, 1999), ventral view, redrawn from Dhanumkumari (1999, fig. 1). 19. A. odhneri (Syn. Astiotrema nathi Gupta, 1954), ventral view, redrawn from Gupta (1954, fig. 1). 20. A. odhneri (Syn. Astiotrema sudanensis Khalil, 1959), dorsal view, redrawn from Khalil (1954, fig. 1). Abbreviations: AT, anterior testis; Ce, cecum; CP, cirrus-pouch; Es, esophagus; GP, genital pore; MG, Mehlis’ gland; 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, vasdeferens; VF, vitelline follicle; VS, ventral sucker. Scale bars: Fig. 17 = 1,000 µm; Fig. 18 = 1,000 µm; Fig. 19 = 500 µm; Fig. 20 = 500 µm.