skip to main content


Title: Phylogenetic analysis and diversity of peculiar new lecanicephalidean tapeworms (Eniochobothriidae) from cownose rays across the globe
The three members of the lecanicephalidean tapeworm family Eniochobothriidae are unusual among tapeworms in that they lack a vagina and possess a series of expanded proglottids forming a trough at the anterior end of their body. They exclusively parasitise cownose rays of the genus Rhinoptera (Myliobatiformes: Rhinopteridae). New collections from six of the nine known species of cownose rays from the waters off Australia, Mexico, Mozambique, Senegal, Taiwan and the United States (off Mississippi, Louisiana and South Carolina) yielded eight new species and a new genus of eniochobothriids. Here we erect Amiculucestus, gen. nov. and describe six of the eight new species – four in the new genus and two in Eniochobothrium – expanding the number of genera in the family to two and the number of described species in the family to nine. Morphological work was based on light and scanning electron microscopy. The tree resulting from a maximum likelihood analysis of sequence data for the D1–D3 region of the 28S rDNA gene for 11 species of eniochobothriids supports the reciprocal monophyly of both genera. The mode of attachment to the mucosal surface of the spiral intestine of the host was investigated using histological sections of worms in situ. These cestodes appear to use the anterior trough-like portion of their body, which consists of an unusual series of barren proglottids, rather than their scolex, to attach to the mucosal surface. Based on our new collections, we estimate that the total number of eniochobothriids across the globe does not exceed 27 species. ZooBank LSID: urn:lsid:zoobank.org:pub:0740EC72‐AC3F‐43AA‐BD41‐B9820BA9D0CE  more » « less
Award ID(s):
1921404 1921411
NSF-PAR ID:
10448718
Author(s) / Creator(s):
;
Editor(s):
Worsaae, Katrine
Date Published:
Journal Name:
Invertebrate Systematics
Volume:
36
Issue:
10
ISSN:
1445-5226
Page Range / eLocation ID:
879 to 909
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Since 2010, the trypanorhynch tapeworm family Rhinoptericolidae Carvajal & Campbell, 1975 has housed just two distinctive, monotypic genera ( Rhinoptericola Carvajal & Campbell, 1975 and Nataliella Palm, 2010). However, global collections of tapeworms from sharks and rays over the last more than three decades brought to light the need for major revision of the family by suggesting a much greater species-level diversity for the nominal genus Rhinoptericola . Through synonymy and the description of new species, the number of species in the genus is increased from one to eight. A phylogenetic analysis of the D1–D3 gene region of 28S rRNA (28S), including seven of the now nine species of rhinoptericolids, and a broad sampling of the other Trypanobatoida is the first to recover a monophyletic Rhinoptericolidae. In addition to systematic revision, this study allowed for the first evaluation of the degree of intraspecific vs interspecific variation in 28S for adult trypanorhynchs across the various hosts and geographic localities from which they have been reported, suggesting a relatively consistent boundary for Rhinoptericola . It is further suggested that detailed scanning electron microscopy (SEM) images of both the basal and metabasal armatures greatly aid in the interpretation of hook arrangement and shape. A schematic to streamline determination of the tentacular surface presented in scanning electron micrographs and line drawings of trypanorhynchs is presented for species with both two and four bothria. In combination, these methodological refinements can now be used as a model to resolve issues of classification and non-monophyly within both major lineages of the Trypanorhyncha. As a result of the taxonomic work, Rhinoptericola megacantha Carvajal & Campbell, 1975 (previously only known from the American cownose ray from the Chesapeake Bay and the Ticon cownose ray from the Gulf of Mexico, Venezuela, and Brazil) is now known from an additional species of cownose ray and a species of stingray, and is revealed to have a transatlantic distribution. Data from SEM suggest a simpler interpretation of hook arrangement in the metabasal armature for Rhinoptercola and—in combination with 28S sequence data—support Shirleyrhynchus Beveridge & Campbell, 1988 (a former rhinoptericolid) as its junior synonym. The three species formerly assigned to Shirleyrhynchus are thus transferred to Rhinoptericola . Data from light microscopy on whole-mounted specimens and histological sections, SEM, and 28S showed the eutetrarhynchid Prochristianella jensenae Schaeffner & Beveridge, 2012b to be morphologically consistent with species of Rhinoptericola and it is thus transferred to the genus. The type series of P. jensenae was determined to be mixed, representing two distinct species which are here redescribed and described as new, respectively. Two additional novel species of Rhinoptericola are described from cownose rays from off Mozambique and the Gulf of California. 
    more » « less
  2. The Rhoptrobothriidae are one of the more enigmatic families of cestodes of elasmobranchs. Opinions on the taxonomic status of the family’s three original genera (i.e., Myzophyllobothrium, Rhoptrobothrium, and Myzocephalus) have varied over the 115 years since they were erected. Some authors have considered all three valid, others have considered Rhoptrobothrium to be a synonym of Myzopyllobothrium or a genus inquirendum, yet others have considered Myzocephalus to be a synonym of the phyllobothriid genus Thysanocephalum. All three genera were established for specimens collected from eagle rays off Sri Lanka. The erection of Mixophyllobothrium for two specimens from a cowtail stingray off India three decades ago added additional confusion to the situation, with some authors considering it valid and others a synonym of Myzocephalus. These disagreements stem largely from differences in interpretation of the complex morphology of the scolex of members of these genera. Furthermore, with the exception of Rhoptrobothrium comprising four species, each genus is monotypic. All but Rhoptrobothrium has not been considered in detail for nearly a century, largely because of a lack of available material. The taxonomic status of these genera is assessed here based on light and scanning electron microscopy, and molecular data generated from new material collected from eagle rays off Indonesian and Malaysian Borneo, Japan, Sri Lanka, and Viet Nam. Morphological work indicates that the genera differ largely only in the degree of folding of the four remi that extend from the cephalic peduncle. A molecular phylogeny based on sequence data for the D1–D3 region of the 28S rRNA gene, which include new data for eight specimens of four species, indicates that Myzophyllobothrium, Myzocephalus, and Rhoptrobothrium are not mutually monophyletic. The latter two genera and Mixophyllobothrium are considered synonyms of Myzophyllobothrium and five species are transferred to that genus. Myzophyllobothrium okamuri n. comb. is considered a species inquirendum. Myzophyllobothrium nagasawai n. sp. is described from Aetobatus narutobiei off Japan. Myzophyllobothrium narinari n. comb. is re-described based on newly collected cestodes from the type host and locality (i.e., Aetobatus ocellatus off Sri Lanka). Despite consisting of only a single genus, the family status of the group is retained in recognition of the unusual configuration of the scolex, which bears four biloculate bothridia and four remi extending from the cephalic peduncle. The ordinal placement of the family remains uncertain, but affinities with the Phyllobothriidea, rather than “Tetraphyllidea” are considered. 
    more » « less
  3. null (Ed.)
    Two new species of the cestode genus Caulobothrium, collected from the duckbill eagle ray, Aetomylaeus bovinus, off Senegal, are described. Although postulated as sister taxa in an earlier molecular phylogenetic analysis, Caulobothrium multispelaeum n. sp. and Caulobothrium katzi n. sp., respectively, are among the smallest and largest members of the genus. The smaller species is unique among its congeners in possessing unusual medial longitudinal grooves along the dorsal and ventral surfaces of its strobila that develop into a tandem series of elliptical apertures on the posterior proglottids. The inner surfaces of these apertures stained positively with McManus’ periodic acid Schiff in a manner similar to that seen in members of the distantly related lecanicephalidean genus Elicilacunosus. The larger species differs from its congeners in size, number of proglottids, and arrangement of bothridial loculi. Both new species were found to possess a small apical sucker on the anterior margin of each of their bothridia. Scanning electron microscopy (SEM) and frontal sections of a bothridium of Caulobothrium tetrascaphium suggests that this species also bears an apical sucker. Examination of the hologenophore of the species provisionally referred to as Caulobothrium n. sp. 5 in the earlier molecular analysis indicates it is conspecific with the recently described Caulobothrium pedunculatum, which was also determined to possess bothridial apical suckers. This leads us to suspect that this feature may be found to occur in all members of the genus. SEM of specimens of Caulobothrium for the first time indicates their bothridial surfaces are covered with filitriches of various sizes but lack spinitriches; spinitriches were seen only on the cephalic peduncle of C. katzi n. sp. The geographic distribution and host associations of Caulobothrium are expanded to include data now available for all species. The diagnosis of the genus is revised to include all of this information. 
    more » « less
  4. Abstract

    The diverse, largely Neotropical subtribe Euptychiina is widely regarded as one of the most taxonomically challenging groups among all butterflies. Over the last two decades, morphological and molecular studies have revealed widespread paraphyly and polyphyly among genera, and a comprehensive, robust phylogenetic hypothesis is needed to build a firm generic classification to support ongoing taxonomic revisions at the species level. Here, we generated a dataset that includes sequences for up to nine nuclear genes and the mitochondrial COI ‘barcode’ for a total of 1280 specimens representing 449 described and undescribed species of Euptychiina and 39 out‐groups, resulting in the most complete phylogeny for the subtribe to date. In combination with a recently developed genomic backbone tree, this dataset resulted in a topology with strong support for most branches. We recognize eight major clades that each contain two or more genera, together containing all but seven Euptychiina genera. We provide a summary of the taxonomy, diversity and natural history of each clade, and discuss taxonomic changes implied by the phylogenetic results. We describe nine new genera to accommodate 38 described species:LazulinaWillmott, Nakahara & Espeland,gen.n.,SauronaHuertas & Willmott,gen.n.,ArgentariaHuertas & Willmott,gen.n.,TaguaibaFreitas, Zacca & Siewert,gen.n.,XenovenaMarín & Nakahara,gen.n.,DeltayaWillmott, Nakahara & Espeland,gen.n.,ModicaZacca, Casagrande & Willmott,gen.n.,OccultaNakahara & Willmott,gen.n., andTricoNakahara & Espeland,gen.n.We also synonymizeNubilaViloria, Andrade & Henao, 2019 (syn.n.) withSplendeuptychiaForster, 1964,MacrocissiaViloria, Le Crom & Andrade, 2019 (syn.n.) withSatyrotaygetisForster, 1964, andRudyphthimoidesViloria, 2022 (syn.n.) withMalaveriaViloria & Benmesbah, 2020. Overall, we revised the generic placement of 79 species (74 new generic combinations and five revised combinations), and as a result all but six described species of Euptychiina are accommodated within 70 named, monophyletic genera. For all newly described genera, we provide illustrations of representative species, drawings of wing venation and male and (where possible) female genitalia, and distribution maps, and summarize the natural history of the genus. For three new monotypic genera,Occultagen.n.,Tricogen.n.andXenovenagen.n.we provide a taxonomic revision with a review of the taxonomy of each species and data from examined specimens. We provide a revised synonymic list for Euptychiina containing 460 valid described species, 53 subspecies and 255 synonyms, including several new synonyms and reinstated species.

     
    more » « less
  5. This paper aims to expand understanding of a poorly known group of cestodes that parasitize an intriguingly diverse suite of elasmobranchs. The group’s three currently described members (i.e., Pentaloculum macrocephalum, Pentaloculum hoi, and Zyxibothrium kamienae) parasitize an electric ray, a carpet shark, and a skate, respectively. Pentaloculum grahami n. sp. is described from a second genus of carpet shark, specifically Parascyllium collare, in Australia. Zyxibothrium duffyi n. sp. and Zyxibothrium healyae n. sp. are described from the deep-sea skates Brochiraja asperula and Brochiraja spinifera, respectively off New Zealand. The three new species share distinctive bothridia that bear a small number of large, circular, facial loculi and lateral bands of vitelline follicles that converge posterior to the ovary—features which are found in all other members of these genera. Zyxibothrium healyae n. sp. is unique in possessing three, rather than four or five, facial loculi. Zyxibothrium duffyi n. sp. possesses a combination of five facial loculi and vitelline follicles that stop short of the anterior margin of the proglottid. Pentaloculum grahami n. sp. is the largest member of the group with the greatest number of proglottids. Based on striking similarities in scolex morphology, Pentaloculum and Zyxibothrium have been hypothesized to belong to a distinct subgroup of “tetraphyllideans” provisionally designated as Clade 1. Based on sequence data for the D1–D3 region of the 28S rDNA gene generated for species of Zyxibothrium for the first time, we confirm the reciprocal monophyly of both genera as well as the monophyly of Clade 1 and its status as a distinct lineage among the “Tetraphyllidea”. This work also suggests that the presence of five facial loculi is homoplasious given this character state is found in members of both genera. The new species expand the host associations of Clade 1 to include additional skate and carpet shark genera. Moving forward we would expect to find additional members of this group parasitizing other species of parascyliid carpet sharks as well as other species of the rajid genus Malacoraja and the arhynchobatid genus Brochiraja. Here we have doubled the number of described species in the taxon referred to as Clade 1 while simultaneously expanding our understanding of the morphology and anatomy of its members. This additional information will help inform the ultimate revision of the ordinal classification of the cestodes to address the highly polyphyletic nature of the order “Tetraphyllidea” as it is currently configured. 
    more » « less