PODOCOTYLINAE DOLLFUS, 1959

Martin, Storm Blas, Huston, Daniel Colgan, Cutmore, Scott Christopher & Cribb, Thomas Herbert, 2019, A new classification for deep-sea opecoelid trematodes based on the phylogenetic position of some unusual taxa from shallow-water, herbivorous fishes off south-west Australia, Zoological Journal of the Linnean Society 186, pp. 385-413 : 404-405

PODOCOTYLINAE DOLLFUS, 1959

Diagnosis: Body oval, fusiform, pyrifrom or elongate-oval, dorso-ventrally flattened, medium to large. Tegument smooth. Forebody less than one-half body length. Oral sucker unspecialized or funnel-shaped. Ventral sucker larger than oral sucker, sessile to protuberant. Pharynx unspecialized. Prepharynx short. Oesophagus unspecialized. Intestine bifurcates in forebody or dorsal to ventral sucker. Caeca blind, terminate near posterior extremity. Testes two, smooth or lobed, medial or diagonal, separate or contiguous. Cirrus-sac usually well developed, may be absent, restricted to forebody or overlapping ventral sucker or extending into hindbody. Seminal vesicle, usually internal, sometimes naked, usually long, thin and sinuous distally. Pars-prostatica present, may be inconspicuous. Ejaculatory duct often short. Common genital atrium simple. Genital pore bifurcal or pre-bifurcal, sinistro-submedial. Ovary smooth to regularly or irregularly lobed, medial to dextro-submedial, smaller than and anterior to testes, contiguous with or separate from anterior testis, separate from ventral sucker. Seminal receptacle canalicular. Laurer’s canal present. Mehlis’ gland present. Uterus preovarian. Vitellarine follicles always extending beyond testes posteriorly, entering forebody or restricted to hindbody, may be distributed ventrally and dorsally or absent dorsally. Eggs oval, operculate, unembryonated in utero, without filaments or protuberances. Excretory vesicle tubular, extends to level of ovary. Excretory pore terminal. In Antarctic, sub-Antarctic and deep-sea, especially bathypelagic, fishes, several families.

Type-genus: Podocotyle Dujardin, 1845

Other genera: Bathypodocotyle gen.nov., Buticulotrema Dronen & McEachran, 1993 ; Halosaurotrema gen. nov.; Macrourimegatrema Blend et al., 2004 ; Neolebouria Gibson, 1976 ; Tellervotrema Gibson & Bray, 1982 .

Remarks: Dollfus (1959) proposed the Podocotylidae and Podocotyloidea, but most subsequent authors have considered Podocotyle , the type-genus, to belong in the Opecoelidae . Nevertheless, as per the principle of coordination, Dollfus (1959) also established the subfamily name, the Podocotylinae . Here, this subfamily concept is resurrected for Podocotyle , as well as Bathypodocotyle , Buticulotrema , Halosaurotrema and Neolebouria , each of which is represented in phylogenetic analyses by a single species and together form a strongly supported clade ( Fig. 1). We also include Macrourimegatrema and Tellervotrema in this concept. These genera comprise two and three species, respectively, none of which are represented by sequence data. Collectively, podocotyline taxa are almost all known from deep-sea and/or temperate to polar fishes. Species of Bathypodocotyle , Buticulotrema , Macrourimegatrema and Tellervotrema occur in gadiform fishes, specifically of the Macrouridae and mainly in the north Atlantic; one species is known from the north Pacific ( Gibson & Bray, 1982; Blend et al., 2004, 2007; Kuramochi, 2009). The sole species of Halosaurotrema is known from a north Atlantic halosaurid (Notocanthiformes) ( Bray & Campbell, 1996), and species of Neolebouria , as recognized here, are known mainly from Antarctic and sub-Antarctic notothenioid perciform fishes; two are also known from a liparid ( Scorpaeniformes ), and a third is known only from an Atlantic ipnopid ( Aulopiformes ) ( Gibson, 1976; Gibson & Bray, 1982; Zdzitowiecki, 1987, 1991, 1997; Zdzitowiecki et al., 1993; Palm et al., 2007). The many, ecologically diverse species of Podocotyle probably represent multiple distinct lineages, but five nominal species, and one unnamed species discussed by Blend et al. (2017), are known only from deep-sea fishes in the north-west Atlantic: four, P. harrissae Bray & Campbell, 1996 , P. nimoyi Blend, Dronen, & Armstrong, 2016 , P. pearsei Manter, 1934 and the unnamed species are from macrourids, one, P. shistotesticulata Bray & Campbell, 1996 , is from a morid, another gadiform fish, and one, P. bathyhelminthos Blend & Dronen, 2015 , from an ophidiid ( Ophidiiformes ) ( Manter, 1934; Bray & Campbell, 1996; Blend & Dronen, 2015b; Blend et al., 2016, 2017). These species are almost certainly closely related to species of Bathypodocotyle and Tellervotrema , differing from the former by a lobed vs. entire ovary and from the latter by restriction of the vitelline field to the hindbody. Perhaps most compellingly, like species of Bathypodocotyle and Tellervotrema , all six species of Podocotyle have a short cirrus-sac (in P. bathyhelminthos it may protrude a little into the hindbody) and a short to exceptionally short ejaculatory duct. Podocotyle atomon , the only sequenced representative of the genus, is known from a variety of fishes, mainly from the north Atlantic, Arctic and north Pacific, including Gadiformes ( Gadidae ), but also Anguilliformes, Gasterosteiformes , Perciformes , Pleuronectiformes , Scorpaeniformes and Sygnathiformes. It resolved as sister to B. margolisi in the phylogenetic analyses ( Fig. 1) and is more consistent with the type species, P. angulata Dujardin, 1845 , than with the Podocotyle species from deep-sea macrourids. Podocotyle angulata is also known from fishes of the Anguilliformes, Gasterosteiformes and Pleuronectiformes in the north Atlantic.

Morphologically, the taxa included here in the Podocotylinae are mostly highly conserved, distinguished from one-another mainly by the distribution of the vitelline follicles, lobation and arrangement of the gonads, and relative lengths of the forebody and hindbody. Thus, similar to the distinctions made for Podocotyle above, the concept of Halosaurotrema differs from that of Neolebouria (s.s) in hindbody length and arrangement of the gonads, Bathypodocotyle differs from Neolebouria (s.s) and Tellervotrema mainly in restriction of the vitelline follicles to the hindbody, and Neolebouria (s.s) and Tellervotrema essentially differ only in the presence vs. absence of a dorsal vitelline field and perhaps in the regularity and degree of ovary lobation. Specialized conditions serve to distinguish two genera: species of Macrourimegatrema have a funnel-shaped oral sucker, and, most significantly, species of Buticulotrema lack a cirrus-sac. Buticulotrema is, therefore, usually considered to belong to the Opecoelininae , but the concept of that subfamily is dubious. Species of Buticulotrema bear no significant resemblance to those of Opecoelina , the type-genus, or Bartoliella Aken’Ova, 2003, the only other nominal genus. Neither includes species known from bathypelagic fishes and both concepts require the caeca to unite and open into a common anus, whereas in species of Buticulotrema the caeca are blind. Sequence data have not yet been generated from specimens related to species of either Opecoelina or Bartoliella , but it seems unlikely that these will prove to be closely related to those of Buticulotrema .

The concept of the Podocotylinae can be distinguished from the Bathycreadinae by blind caeca vs. caeca forming a cyclocoel and from the Opecoelinae and Stenakrinae by a canalicular vs. uterine seminal receptacle. Distinction from the Plagioporinae (s.s), i.e. the freshwater clade, is more subtle, but we think two characters provide a potentially reliable basis. In the Podocotylinae , the excretory vesicle is longer, always reaching to the level of the ovary vs. at most to the level of the testes. Second, in some freshwater plagioporine taxa, the uterus becomes extracaecal and/or post-testicular, whereas in the Podocotylinae it is (almost) always intercaecal and preovarian. Only in one species from deep-sea fishes, Podocotyle nimoyi , is the uterus not strictly preovarian. In this species it extends to between the ovary and the anterior testis and partially dorsal to the anterior testis, but it does not enter the post-testicular zone. Additionally, a short cirrus-sac with a seminal vesicle becoming long or even duct-like distally and, in particular, a short ejaculatory duct occupying less than half the length of the cirrus-sac, appears to unite several podocotyline taxa, specifically species of Bathypodocotyle , Neolebouria , Tellervotrema and some Podocotyle .