Alloastiotrema Karar & Blend & Dronen & Adel 2023, n. gen.

Alloastiotrema n. gen.

(Figs. 12 & 13)

Type- and only species. Alloastiotrema birmanii (Khan, Gul-E-Lala, Ghazi, Khatoon, Waheed & Khan, 2021) n. comb.

(Syn. Astiotrema birmanii Khan, Gul-E-Lala, Ghazi, Khatoon, Waheed & Khan, 2021)

Etymology. The generic designation is based on the Greek word root “allos” meaning “other” or “strange” and refers to differences the new genus has compared to other taxa within Astiotrema Looss, 1900 (sensu lato), wherein one species now composing this genus was originally considered.

Diagnosis. Body large, elongate, spatulate. Tegument spinous. Forebody approximately 1/2 of body length. Suckers subglobular, unspecialized. Oral sucker round, subterminal. Ventral sucker equatorial to immediately post-equatorial, slightly larger than oral sucker. Prepharynx indistinct. Pharynx well developed, smaller than suckers. Esophagus moderately long, thin-walled, straight. Intestinal bifurcation well anterior to ventral sucker at midpoint of first 1/4 of body. Ceca terminate near posterior extremity. Testes two, intercecal, smooth, oblique, elliptical, contiguous or separated by small inter-testicular space. Cirrus-pouch large, clavate, runs straight along longitudinal axis, well anterior to ventral sucker, does not exceed mid-forebody level. Seminal vesicle large, saccular, occupies most of space in cirrus-pouch; pars prostatica and ejaculatory duct short, tubular, indistinct from each other. Genital pore median, conspicuously pre-bifurcal. Ovary trilobed, in posterior half of body, intercecal, submedian. Vitelline follicles small, in two irregular extracecal lateral fields, confined between base of cirrus-pouch and level of anterior margin of ventral sucker. Uterus extra-, inter- and post-cecal; coils confluent anteriorly and fills most space between cirrus-pouch and ventral sucker; occupies entire hindbody posterior to testes. Eggs numerous, elliptical, tanned. Excretory vesicle not observed. Excretory pore terminal. In intestine of bullfrogs (Dicroglossidae Anderson); Southern Asia.

Remarks. Khan et al. (2021) established A. birmanii to accommodate specimens collected from the intestine of the Indian or Indus Valley bullfrog, Hoplobatrachus tigerinus (Daudin) (syn. Rana tigrina Daudin) (Anura: Dicroglossidae), from various localities of Karachi, Sindh, Pakistan. Astiotrema birmanii can be easily distinguished from all taxa of Astiotrema either at the expanded or restricted levels by a combination of the following features: (i) longer forebody, approximately half body length; (ii) an equatorial to immediately post-equatorial ventral sucker; (iii) a large distance, about 1/3 of body length, separating the intestinal bifurcation and ventral sucker; (iv) a trilobed, post-equatorial ovary; (v) vitellarium located anterior to the ventral sucker, confined between the base of the cirrus-pouch and the level of the anterior portion of the ventral sucker; (vi) the cirrus-pouch does not exceed mid-forebody level posteriorly and is well-separated from the ventral sucker by a large distance of about 1/4 of body length; and (vii) the uterus is inter-, post- and extensively extra-cecal with coils confluent anteriorly, filling most space anterior to the ventral sucker and occupying the entire hindbody posterior to the testes (see Khan et al. 2021, figs. 1 & 2). In contrast, taxa of Astiotrema (sensu lato) have: (i) a shorter forebody that does not exceed 1/3 of body length; (ii) a conspicuously pre-equatorial ventral sucker; (iii) a very small distance separating the intestinal bifurcation from the ventral sucker; (iv) an entire, smooth and pre-equatorial to slightly equatorial ovary; (v) vitellarium extending between the base of the oral sucker to the posterior extremity; (vi) a cirrus-pouch that extends distinctly into the hindbody or at least located at the ventral sucker level; and (vii) the uterus is inter- and post-cecal, occasionally slightly extracecal, filling the inter-testicular space and most of hindbody posterior to the ovary, extending to the posterior extremity. Despite the paucity of information provided in the description of A. birmanii by Khan et al. (2021) and their uninformative illustrations (see Khan et al. 2021, figs. 1 & 2), the inferred characteristics and the dissimilar morphological features observed in A. birmanii as well as its distinct host group (Dicroglossidae) provide sufficient evidence to suggest that A. birmanii belongs in neither Astiotrema (sensu stricto) nor its derived genera (Homeoastiotrema, Ichthyastiotrema and Plesioastiotrema).

To our knowledge, investigations on digeneans infecting H. tigerinus reveal that this anuran host represents a repository for Indian digeneans only with the exception of A. birmanii from Pakistan (Khan et al. 2021) and Diplodiscus amphichrus Tubangui, 1933 from the Philippines (Skrjabin 1949). These digeneans include the following: i) Astiotrema ranarum (Mehra & Negi, 1926) Fotedar, 1971 (Karar et al. 2021); ii) Diplodiscus magnus Srivastava, 1934 (Srivastava 1934); iii) Halipegus mehransis Srivastava, 1933 (Chauhan 1953; Skrjabin & Guschanskaja 1955); iv) Halipegus ovocaudatus (Vulpian, 1859) Looss, 1899 (Chauhan 1953); v) Mesocoelium thapari Gupta & Jahan, 1978 (Gupta & Jahan 1978); vi) Phyllodistomum shandrai Bhalerao, 1937 (Bhalerao 1937; Pigulewsky 1953); vii) Pleurogenoides euphlycti Shinad & Prasadan, 2018 (Shinad & Prasadan 2018); viii) Pleurogenoides gastroporus (Lühe, 1901) Travassos, 1921 (Khotenovsky 1970); ix) Pleurogenoides sphaericus (Klein, 1905) Travassos, 1921 (Khotenovsky 1970); and x) Pleurogenoides wayanadensis Shinad & Prasadan, 2018 (Shinad & Prasadan 2018). Astiotrema birmanii is characterized from all previously mentioned digeneans by the same features discussed above as with that of Astiotrema; thus, based on the dissimilar morphological features observed in A. birmanii, we find it also does not belong in any of these close representative genera.

Although Khan et al. (2021) believed A. birmanii to be a plagiorchiid, our findings suggest that A. birmanii is closer to the Dolichoperoididae Johnston & Angel, 1940 rather than the Plagiorchiidae based on the combination of the following characteristics: genital pore median, at level of esophagus; oral sucker lacks lateral muscular papillae or lappets; ventral sucker well-developed, undivided; forebody long; vitelline follicles in continuous fields; and parasitic in an anuran (Bray 2008e; Gibson 2008). Astiotrema birmanii and dolichoperoidids share some morphological characteristics, in particular, a long forebody, a ventral sucker just inside the posterior half of the body, a large distance separating the intestinal bifurcation and ventral sucker, and a post-equatorial ovary. However, members of the latter are distinguished from the former by an elongate-fusiform body; symmetrical or almost so testes; a ventrally sub-lateral genital pore on either side of the body at the level of the oral sucker; a ventral sucker slightly smaller than the oral one; a subglobular ovary; uterine coils that do not reach the post-testicular space; vitellarium in restricted lateral fields between about the level of the ventral sucker and level of the testes; and dolichoperoidids are parasites in the lungs, trachea and esophagus of snakes restricted to Australia (see Gibson 2008). Our investigations suggest A. birmanii is closer to another genus, Caudouterina Martin, 1966, which currently is in a disputed taxonomic position (i.e., this genus has been considered either in the Allocreadiidae [see Martin 1966; Yamaguti 1971; Caira & Bogea 2005] or closer to the Encyclometridae Mehra, 1931 [see Curran et al. 2006]). Both A. birmanii and Caudouterina rhyacotritoni Martin, 1966 parasitize amphibian hosts (Indian or Indus Valley bullfrog, H. tigerinus vs Olympic torrent salamander, Rhyacotriton olympicus [Gaige] [Urodela: Rhyacotritonidae]) and share several morphological features; in particular, a long forebody, a nearly equatorial ventral sucker, a large distance separating the intestinal bifurcation and ventral sucker, and a post-equatorial ovary. However, A. birmanii can be easily distinguished by (i) its trilobed ovary vs entire smooth one in C. rhyacotritoni; (ii) vitellarium confined between base of cirrus-pouch and level of anterior portion of ventral sucker vs vitellarium situated between level of pharynx and near posterior extremity, confluent anterior to ventral sucker; (iii) large cirrus-pouch well-separated from ventral sucker by a large distance vs small one and immediately anterior to/contiguous with ventral sucker; (iv) a genital pore that is pre-bifurcal vs conspicuously posterior to the intestinal bifurcation; and (v) A. birmanii possesses a uterus that is highly extensive extra-cecally with coils confluent anteriorly filling most of the space anterior to the ventral sucker and occupying the entire hindbody posterior to the testes (see Khan et al. 2021, figs. 1 & 2) vs a uterus in C. rhyacotritoni that reaches the posterior extremity with one or more loops extending between testes (see Martin 1966; Caira & Bogea 2005). With the comparatively unique morphological features observed in A. birmanii, we believe this species does not belong in either the Dolichoperoididae or Caudouterina and is in need of its own genus. Therefore, we erect Alloastiotrema n. gen. and designate As. birmanii as its type species, Alloastiotrema birmanii (Khan, Gul-E-Lala, Ghazi, Khatoon, Waheed & Khan, 2021) n. comb. For Alloastiotrema we lack information about the nature and shape of the excretory vesicle, the distribution of spines over the body, and the presence/absence of a seminal receptacle. Therefore, we exclude Alloastiotrema from the family Plagiorchiidae, and while we believe it to belong within the superfamily Plagiorchioidea, its family designation remains uncertain.