HAMACREADIINAE MARTIN, DOWIE & CRIBB, 2020

Martin, Storm Blas, Downie, Abigail Jayne & Cribb, Thomas Herbert, 2020, A new subfamily for a clade of opecoelids (Trematoda: Digenea) exploiting marine fishes as second-intermediate hosts, with the first report of opecoelid metacercariae from an elasmobranch, Zoological Journal of the Linnean Society 188, pp. 455-472 : 464-467

SUBFAMILY HAMACREADIINAE MARTIN, DOWIE & CRIBB SUBFAM. NOV.

Lsid

Diagnosis: Body medium to large, subcylindrical or dorsoventrally flattened and linguiform to elongate-oval. Tegument smooth. Oral sucker usually unspecialized, may be funnel shaped. Ventral sucker sessile and larger than oral sucker or pedunculate and may be smaller than ventral sucker. Prepharynx short. Pharynx smaller than oral sucker. Oesophagus unspecialized. Intestine bifurcates in forebody or Excretory vesicle tubular, may extend into forebody. Excretory pore terminal. Adults in piscivorous marine fishes. Metacercariae developing in fishes, mostly teleosts, sometimes chondrichthyans, and possibly cephalopods.

Type genus: Hamacreadium Linton, 1910 .

Other genera: Allopodocotyle Pritchard, 1966 ; Bentholebouria Andres, Pulis & Overstreet, 2014 ; Cainocreadium Nicoll, 1909 ; Choanotrema Nitta & Tanaka, 2018 ; Pacificreadium Durio & Manter, 1968 ; Paraplagioporus Yamaguti, 1939 ; Pedunculacetabulum Yamaguti, 1934 ; Podocotyloides Yamaguti, 1934 .

dorsal to ventral sucker. Caeca blind, terminate beyond testes near posterior extremity. Testes two, in hindbody, diagonal or tandem. Cirrus sac well developed, subcylindrical to claviform. Seminal vesicle internal, large. Pars prostatica prominent. Ejaculatory duct usually long. Genital atrium often conspicuous. Genital pore ventral, medial or sinistro-submedial, prebifurcal or postbifurcal. Ovary dextro-submedial or medial, smooth to deeply lobed, usually smaller than testes. Canalicular seminal receptacle present, often large, conspicuous. Laurer’s canal opens dorsal to ovarian complex. Vitellarium follicular; follicles extensive, circumcaecal. Uterus arranged into loose, poorly defined coils, intercaecal, often confined to space between gonads and ventral sucker, may extend between testes, with or without metraterm. Eggs without polar filaments. Mehlis’ gland present. Remarks: All opecoelids recognized here in the Hamacreadiinae have been transferred from the previous, much larger definition of the Plagioporinae (i.e. s.l.). Morphologically, hamacreadiines can generally be distinguished from plagioporines by a longer excretory vesicle reaching at least to the level of the ovary and, in many cases, a less extensive uterus, mainly restricted to the intercaecal space between the ventral sucker and the gonads and usually not extending beyond the testes posteriorly. Like the Plagioporinae , the Hamacreadiinae is defined for taxa with a well-developed cirrus sac and a canalicular seminal vesicle, distinguishing the subfamily from the Opecoelinae , Opecoelininae , Polypipapiliotrematinae and Stenakrinae . Hamacreadiines can also be distinguished easily from taxa belonging to the Bathycreadiinae by blind caeca and those of the Helicometrinae by unfilamented eggs and an unspecialized, as opposed to helical, uterus.

No single character or combination of characters reliably distinguishes all hamacreadiine taxa from all those belonging to the Opistholebetinae . However, many, but not all, opistholebetines have a post-oral muscular ring, a forebody composing more than half the body length and/or pigment granules distributed throughout the parenchyma, features unique to that subfamily among the Opecoelidae . Additionally, most opistholebetines are robust, with a thick tegument, and some are pyriform to almost round, whereas hamacreadiines are mostly either large, dorsoventrally flattened and linguiform to elongate-oval, or elongate and subcylindrical with a pedunculate ventral sucker. The Hamacreadiinae is perhaps most similar to the Podocotylinae . There is no clear distinction between the two, although representative taxa are relatively distantly related phylogenetically ( Fig. 3 ) and podocotylines appear mostly to occur in the deep sea and possibly northern, temperate regions. Martin et al. (2019) suggested that some details of the male terminal genitalia might unite the podocotyline taxa, to the exclusion of taxa now considered in the Hamacreadiinae . Specifically, they noted a tendency for the cirrus sac to be small and for the seminal vesicle to become long, thin and sinuous anteriorly. These are hardly strong characters, and further investigation into the bounds of the Podocotylinae is required to improve its morphological definition.

The taxa belonging to the group termed the marine Plagioporinae (s.l.) clade C ( Fig. 3 ) will probably require a subfamily of their own in the near future, although the prospect of establishing a morphological basis for such a concept seems challenging at present. Except for some species with especially small eggs, most of these taxa are especially generalized in morphology and cannot be delineated reliably from the Hamacreadiinae , although generally they are smaller species. They are not included here in the new subfamily on the basis of phylogenetic distinction. Conversely, although Macvicaria macassarensis and Podocotyle scorpaenae (Rudolphi, 1919) Bartoli & Gibson, 1999 resolved in the Hamacreadiinae ( Figs 1 , 3 ), it seems that neither species is a genuine representative of its nominal genus and thus neither Macvicaria nor Podocotyle is included here in the Hamacreadiinae . Both genera are large and polyphyletic, and the type species of Macvicaria Gibson & Bray, 1982 resolves in the Opistholebetinae , whereas Podocotyle Dujardin, 1845 is recognized as the type genus of the Podocotylinae on the basis of sequence data for Podocotyle atomon (Rudolphi, 1802) Odhner, 1905 .

Hamacreadium is selected as the type genus for the new subfamily, because the genus is typical of the clade, it has recently been revised ( Martin et al., 2017b) and its type species, H. mutabile , is well known, sequenced ( Andres et al., 2014a) and was the first opecoelid known to use fishes as second-intermediate hosts ( Table 1; McCoy, 1929).

Figures

Figure 1. Midpoint-rooted neighbour-joining analysis of partial 5.8S-ITS2–partial 28S rDNA data for Hamacreadiinae, including those generated from metacercariae (M) and cercariae (C), with Polypipapiliotrema stenometra (Polypipapiliotrematinae) forming the outgroup. New sequence data are in bold. References for all GenBank accession numbers are provided in Table 1. Nodal supports are from 1000 bootstrap pseudoreplicates. Evolutionary distances were computed using the number of differences, and the scale bar indicates the number of substitutions per sequence, across 436 bp.

Figure 3. The pylogenetic pattern of second-intermediate host groups, including Amphipoda, Cephalopoda, Chondricthyes, Decapoda, Echinoidea, Gastropoda, Hirudinea, Insecta, Oligochaeta and Osteichthyes, exploited by the Opecoelidae, constructed through maximum likelihood analysis of partial 28S ribosomal DNA data, with two brachycladioids forming the outgroup. Taxa in collapsed clades and GenBank accession numbers for all taxa are listed in Table 3. New sequence data are in bold. Support values <50% are omitted. Scale bar indicates the number of substitutions per site.