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Redescription of Testudotaenia testudo (Magath, 1924) (Eucestoda: Proteocephalidea), a parasite of Apalone spinifera (Le Sueur) (Reptilia: Trionychidae) and Amia calva L. (Pisces: Amiidae) in North America and erection of the Testudotaeniinae n. subfam
Abstract and Figures
Testudotaenia testudo (Magath, 1924) is redescribed from the intestine of the softshell turtle Apalone spinifera (Le Sueur) (Trionychidae) and the bowfin Amia calva Linnaeus (Amiidae) from Reelfoot Lake, Tennessee, United States. A new subfamily, the Testudotaeniinae, is erected. The new taxon differs from all proteocephalidean subfamilies in the position of the genital organs in relation to the longitudinal internal musculature, i.e. the testes are cortical, rarely medullary; the ovary is partly medullary, with cortical lobes; the vitelline follicles are mainly medullary, with some follicles in the cortex; and the uterus is cortical. A key to the subfamilies of the order Proteocephalidea Mola, 1928 is provided. The most characteristic features of T. testudo are the precocious uterine aperture, the presence of internal uterine pores (as previously described for Proteocephalus paraguayensis (Rudin, 1917)), the eggs laid unripe, the very long strobila (up to 970 mm), and the presence of an anterior circular musculature in the suckers, which is considered as a good differential character. Three other species were found in Amia calva: Proteocephalus perplexus La Rue, 1911, P. ambloplitis (Leidy, 1887) and a new, undescribed form. Sequences of the partial nuclear 28S rRNA gene of specimens of T. testudo from Apalone spinulifera and Amia calva confirm the conspecificity of samples from these two very distinct hosts, which may represent a capture phenomenon. As the subfamily Adenobrechmoinae Bursey, Goldberg & Kraus, 2006 and the genus Adenobrechmos Bursey, Goldberg & Kraus, 2006 are based on the presence of an apical organ, a character which reflects a rather common convergence, we consider the Adenobrechmoinae to be a junior synonym of the Proteocephalinae La Rue, 1911 and Adenobrechmos a junior synonym of Ophiotaenia La Rue, 1911. Adenobrechmos greeri Bursey, Goldberg & Kraus, 2006 thus becomes Ophiotaenia greeri (Bursey, Goldberg & Kraus, 2006) n. comb.
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Supplementary resources (9)
Nucleotide Sequence
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... Laruella perplexa somewhat resembles P. ambloplitis, a parasite of bass (Micropterus spp.), which has also been reported from gars and ictalurids (La Rue, 1914;Freze, 1965;de Chambrier et al., 2009). Even the species name perplexus was proposed by La Rue (1911,1914) because it was difficult to differentiate it from P. ambloplitis. ...
... However, a critical review of the literature, together with results of the authors' own examination of bowfin from three U.S. states, made it possible to reduce the list of true (actual, i.e., non-accidental) cestode parasites of A. calva to only three: L. perplexa and two species of Haplobothrium, even though the validity of H. bistrobilae is doubtful. In contrast, de Chambrier et al. (2009), using molecular data, were able to identify a putative new proteocephalid in bowfin from Tennessee. It is possible, if not likely, that future studies of this ancient and fascinating relict in drainages across its range will discover a greater diversity of bowfin tapeworms than is currently known. ...
A new genus, Laruella n. gen., is proposed for the proteocephalid cestode L. perplexa (La Rue, 1911) n. comb. (syn. Proteocephalus perplexus La Rue, 1911), a parasite of a ‘living fossil’, the bowfin (Amia calva), in North America. The new genus is differentiated from other proteocephalid genera by having a massive four-lobed scolex without an apical organ and bearing suckers possessing tear-shaped sphincters on their inner rim, vitelline follicles forming L-shaped lateral fields, with the vitellarium turned inwards (medially) ventrally alongside the posterior margin of the ovary, a ring-like vaginal sphincter situated at a considerable distance from the genital atrium, and ellipsoid eggs resembling those of bothriocephalid and diphyllobothriid tapeworms, except for the absence of an operculum. Phylogenetic relationships of the new genus are not resolved, but it belongs to the so-called Neotropical clade of the Proteocephalidae, which is composed mainly of Neotropical tapeworms of siluriforms and other teleosts, but also Nearctic and Palaearctic species of Ophiotaenia La Rue, 1911 from snakes and amphibians. A morphologically similar species, Proteocephalus ambloplitis (Leidy, 1887) from bass (Micropterus spp.) in North America, is provisionally retained in Proteocephalus Weinland, 1858 because its relationships to L. perplexa are not yet clear. The former species differs from L. perplexa by the presence of a large apical organ, large, elongate vaginal sphincter situated near the genital atrium, vitelline follicles limited to lateral longitudinal fields, strongly coiled vas deferens within the cirrus-sac, and a convoluted vaginal canal anterior to the ovarian isthmus. Laruella perplexa reportedly has a s broad spectrum of hosts but most are likely postcyclic or accidental hosts. A list of cestode parasites reported from bowfin is provided; it includes eight species and three taxa not identified to the species level. However, only three adult cestodes, L. perplexa and two species of Haplobothrium Cooper, 1914, are typical tapeworm parasites of bowfin, but previous molecular studies indicate possible existence of a putative new species in bowfin.
... This colonization event launched a remarkable radiation of one of its constituent families, Proteocephalidae La Rue, 1911, across every landmass except Antarctica . Phylogenetic studies on proteocephalids [called Onchoproteocephalidea I in Caira & Jensen (2017)] based mainly on the nuclear large subunit ribosomal RNA gene (lsrDNA or 28S rDNA) sequences (de Chambrier et al., 2008(de Chambrier et al., , 2009Scholz et al., 2011Scholz et al., , 2013) not only cast doubt on the validity of the current classification of these tapeworms, but also revealed the limitations of conventional views about their evolutionary history and biogeography . These phylogenetic studies also highlighted the key role of Gangesiinae Mola, 1929, one of the 14 recognized subfamilies of Proteocephalidae, in understanding the early diversification of the family. ...
The diversification of tapeworms of the subfamily Gangesiinae (Cestoda: Proteocephalidae), parasites of catfishes (order Siluriformes), is assessed using molecular and morphological evidence. A two-gene (lsrDNA and COI) phylogenetic analysis of all species of Gangesiinae (except Gangesia margolisi) resulted in a basal polytomy that included several lineages of Gangesiinae and Acanthotaeniinae. Palaeogeological events, along with host-shifting and dispersal, played prominent roles in the evolution of these tapeworms. Gangesia radiated through two major lineages in the Indomalayan and Palaearctic regions. Morphological changes during this radiation also included secondary loss of diagnostic morphological features of the genus, as in Gangesia mukutmanipurensis sp. nov., which lacks hooks and hooklets on its scolex. An updated key to the genera placed in Gangesiinae is provided and two new synonyms are proposed. A basal polytomy involving some of the potentially oldest lineages of Gangesiinae prevents firm conclusions regarding the ancestral area of origin of these tapeworms. Nevertheless, when the distribution and host-associations of Gangesiinae are considered in the context of the historical biogeography of their catfish hosts, the Indomalayan region appears to have been the ancestral homeland and a major centre of diversification of these tapeworms, with range expansions in western and northern parts of Eurasia and Africa.
... Some species, such as Proteocephalus fluviatilis Bangham, 1925 andProteocephalus pinguis La Rue, 1911, are closely related to Palearctic taxa of the Proteocephalus-aggregate proposed by de Chambrier et al. (2004). In contrast, other species including Proteocephalus ambloplitis (Leidy, 1887) from centrarchids, bowfin (Amia calva), and ictalurids (Siluriformes: Ictaluridae), and Proteocephalus perplexus La Rue, 1911, from bowfin, are more closely related to Neotropical proteocephalids (de Chambrier et al., 2004(de Chambrier et al., , 2009(de Chambrier et al., , 2015Hypsˇa et al., 2005). ...
In the present paper, species of the Proteocephalus-aggregate de Chambrier, Zehnder, Vaucher, and Mariaux, 2004 (Cestoda: Proteocephalidae) reported from centrarchid and percid fishes in North America are reviewed, and their taxonomic status is critically assessed based on a study of type specimens and new material from Canada and the United States. The following 3 species, supposedly strictly specific to their fish definitive hosts, are recognized as valid: (1) Proteocephalus fluviatilis Bangham, 1925 (new synonyms Proteocephalus osburni Bangham, 1925 and Proteocephalus microcephalus Haderlie, 1953 ; Proteocephalus 'robustus' nomen nudum) from the smallmouth and largemouth bass, Micropterus dolomieu (Lacépède) (type host) and Micropterus salmoides (Lacépède) (both Centrarchidae); (2) Proteocephalus luciopercae Wardle, 1932 (new synonym Proteocephalus stizostethi Hunter and Bangham, 1933 ) from the walleye, Sander vitreus (Mitchill) (type host), and sauger, Sander canadensis (Griffith et Smith) (Percidae); and (3) Proteocephalus pearsei La Rue, 1919 , a parasite of the yellow perch, Perca flavescens Mitchill (Percidae). All species are illustrated based on new, properly heat-fixed material. Scanning electron micrographs of the scoleces of percid tapeworms P. luciopercae and P. pearsei, as well as the bass tapeworms P. fluviatilis and Proteocephalus ambloplitis ( Leidy, 1887 ), the latter of which does not belong to this Proteocephalus-aggregate, are provided for the first time together with a simple key to species identification of proteocephalids from centrarchiform and perciform teleost fishes.
... Some species, such as Proteocephalus fluviatilis Bangham, 1925 andProteocephalus pinguis La Rue, 1911, are closely related to Palearctic taxa of the Proteocephalus-aggregate proposed by de Chambrier et al. (2004). In contrast, other species including Proteocephalus ambloplitis (Leidy, 1887) from centrarchids, bowfin (Amia calva), and ictalurids (Siluriformes: Ictaluridae), and Proteocephalus perplexus La Rue, 1911, from bowfin, are more closely related to Neotropical proteocephalids (de Chambrier et al., 2004(de Chambrier et al., , 2009(de Chambrier et al., , 2015Hypsˇa et al., 2005). ...
In the present paper, species of the Proteocephalus-aggregate de Chambrier, Zehnder, Vaucher, and Mariaux, 2004 (Cestoda: Proteocephalidae) reported from centrarchid and percid fishes in North America are reviewed, and their taxonomic status is critically assessed based on a study of type specimens and new material from Canada and the United States. The following 3 species, supposedly strictly specific to their fish definitive hosts, are recognized as valid: (1) Proteocephalus fluviatilisBangham, 1925 (new synonyms Proteocephalus osburniBangham, 1925 and Proteocephalus microcephalusHaderlie, 1953; Proteocephalus 'robustus' nomen nudum) from the smallmouth and largemouth bass, Micropterus dolomieu (Lacépède) (type host) and Micropterus salmoides (Lacépède) (both Centrarchidae); (2) Proteocephalus luciopercaeWardle, 1932 (new synonym Proteocephalus stizostethiHunter and Bangham, 1933) from the walleye, Sander vitreus (Mitchill) (type host), and sauger, Sander canadensis (Griffith et Smith) (Percidae); and (3) Proteocephalus pearseiLa Rue, 1919, a parasite of the yellow perch, Perca flavescens Mitchill (Percidae). All species are illustrated based on new, properly heat-fixed material. Scanning electron micrographs of the scoleces of percid tapeworms P. luciopercae and P. pearsei, as well as the bass tapeworms P. fluviatilis and Proteocephalus ambloplitis (Leidy, 1887), the latter of which does not belong to this Proteocephalus-aggregate, are provided for the first time together with a simple key to species identification of proteocephalids from centrarchiform and perciform teleost fishes.
Testudotaenia sp. WL-2016 (Platyhelminthes, Cestoda), as a member of Onchoproteocephalidea, was isolated from Pelodiscus sinensis in our previous study in 2016 (GenBank: KU761587.1). It was a new tapeworm found in China, and the only mitochondrial DNA of Testudotaenia reported worldwide. Traditional classification methods are challenging to identify specific cestode species rapidly for performing taxonomic research and disease control studies.We annotated the mitochondrial genome based on the previous sequencing, including analyses of nucleotide composition, codon usage. Ka/Ks, p‑distance, the nucleotide and amino acid similarity of the mitochondrial genomes of Dipylidium caninum, Digramma interrupta, Spirometra erinaceieuropaei, Testudotaenia sp. WL-2016 were analyzed and compared. Testudotaenia sp. WL-2016 and 65 others related cestodes were used to construct a phylogenetic tree with 10 common genes. We chose the trnG and COX3 genes to design specific PCR primers for identification. Testudotaenia sp. WL-2016 was strongly skewed away from A and biased towards G (AT skew= −0.292, GC skew= 0.22). Corresponding to the high T content (42.71%), codons also show relatively high T bias. Both Ka/Ks and p‑distance were less than 1. Data from the mitochondrial genome of Testudotaenia sp. WL-2016 is also valuable for species identification, phylogenies, and biogeography studies. The specific PCR primers enabled us to identify Testudotaenia sp. WL-2016 rapidly and accurately at the molecular level, thus providing a basis for classification and identification.
An updated checklist of tapeworms (Platyhelminthes: Cestoda) that parasitize wild North American amphibians and reptiles is presented: A total of 58 species grouped in 15 genera, 5 families, and 3 orders, are registered: these infect a total of 90 species of reptiles and 88 species of amphibians in the region. An illustrated identification key for the families and genera listed is proposed.
One of the most widely distributed African freshwater fish is the African sharptooth catfish Clarias gariepinus (Burchell) that is naturally distributed in 8 of the 10 ichthyofaunal regions of this continent. Clarias gariepinus is a highly valued and cheap staple to local communities and an ideal aquaculture species. Consequently, interest in the parasitic communities of C. gariepinus has increased as parasites may accidentally be ingested by humans when eating uncooked fish or can be introduced into culture systems through fish stocks supplied from local rivers which affect yield, growth, and marketability. This review provides an overview of the ∼107 metazoan parasite species known to parasitise C. gariepinus in Africa and their general life cycles, morphology, paratenic and post-cyclic infections, and the biogeography and validity of records are discussed. A brief overview is included on the application of some of these parasites in environmental studies and their link to human health.
Ictalurid catfishes (Siluriformes) in North America harbor proteocephalid tapeworms of the subfamily Corallobothriinae. Type species of 2 of 3 genera of these tapeworms from ictalurids are redescribed, based on museum and newly collected material. Essexiella fimbriata (Essex, 1928) is typified mainly by a wide, umbrella-shape scolex with a metascolex formed by numerous folds of tissue, anteriorly directed suckers without sphincters, vitellarium bent inwards posteriorly, 'flower-shaped' uterus (with anterior, lateral and posterior diverticula), and a conspicuously pre-equatorial genital atrium. Verified records of this cestode are only from 3 species of Ictalurus Rafinesque, 1820. Megathylacoides giganteum (Essex, 1928), which seems to be specific to the channel catfish (Ictalurus punctatus), possesses a globular scolex, with a weakly developed metascolex formed by tissue-folds posterior to the suckers, anterolaterally directed suckers with large semilunar sphincters, proglottids that are widest at the level of the genital atrium at the anterior third of the proglottid, and uterine diverticula that do not reach the vitelline follicles laterally. A new subfamily, Essexiellinae Scholz and Barčák, is proposed to accommodate species of Essexiella Scholz, de Chambrier, Mariaux and Kuchta, 2011 (type genus), Megathylacoides Jones, Kerley and Sneed, 1956, and Corallotaenia Freze, 1965 from ictalurid catfishes in the Nearctic Region. These tapeworms possess a metascolex, medullary genital organs, uterus lined with numerous chromophilic cells, pre-equatorial genital atrium, and uterine development of type 2. The new subfamily was monophyletic in all molecular phylogenetic analyses, being most closely related to three Neotropical proteocephalids from the redtail catfish, Phractocephalus hemioliopterus (Bloch and Schneider, 1801), but distant from all remaining proteocephalid tapeworms from freshwater fishes in North America.
Ophiotaenia gilberti sp. n. is described from the intestine of the colubrid snake, Thamnodynastes pallidus (Linnaeus, 1758) (Serpentes: Xenodontinae), from Paraguay. The new species differs from most species of New World members of Ophiotaenia in possessing an apical organ. It differs from the six species possessing an apical organ by a smaller scolex diameter (140-145 versus more than 480) and by a smaller number of testes (57-91 versus more than 107). In all Ophiotaenia with two separate testes fields parasites of New World snakes, the ovary is small, occupying a surface five times smaller (in relation to the proglottis surface) than in most Proteocephalus parasites of Palaearctic fishes. This new character may become important in Proteocephalidea systematics. Because of the presence of two separate testicular field, preformed uterus and smaller ovary surface/proglottis surface ratio, we transfer the following Proteocephalus species parasite of snakes to Ophiotaenia: Proteocephalus arandasi Santos & Rolas, 1973 becomes Ophiotaenia arandasi new combination; P. azevedoi de Chambrier & Vaucher, 1992 becomes O. azevedoi new combination; P catzeflisi de Chambrier & Vaucher, 1992 becomes O. catzeflisi new combination; P. euzeti de Chambrier & Vaucher, 1992 becomes O. euzeti new combination; P. joanae de Chambrier & Paulino, 1997 becomes O. joanae new combination; P. micruricola Shoop & Corkum, 1982 becomes O. micruricola new combination and P. variabilis Brooks, 1978 becomes O. variabilis new combination.
Type material of the proteocephalidean cestode Ophiotaenia hylae Johnston, 1912 is redescribed. It is characterised by a globular scolex with uniloculate suckers, a prominent apical organ covered by spiniform microthriches and containing round to oblong cells of finely granular cytoplasm, and by the internal longitudinal musculature composed by 4-5 dorsal and 4-5 ventral bundles of fibres. A similar taxon, Ophiotaenia sp. from a closely related host species, Litoria moorei, is also studied and compared.
Brooksiella praeputialis (Rego, Santos & Silva, 1974) and Goezeella siluri Fuhrmann, 1916 from the Amazonian siluriform fish Cetopsis coecutiens (Siluriformes: Cetopsidae) are redescribed. Goezeella piramutab Woodland, 1933 is considered as a synonym of Goezeella siluri. Goezeella siluri sensu Brooks & Rasmussen, 1984 becomes Goezeella danbrooksi sp. n., differing from G. siluri by the vitelline follicles position (only dorsal, not lateral), size (much smaller in type material) and shape (slightly wider posteriorly); by the position of vaginal sphincter (which is terminal in G. siluri) and by the number of testes.
A new species of Proteocephalus, P. joanae sp. n., is described from the intestine of the colubrid snake, Xenodon neuwiedi (Gunther, 1863) (Serpentes: Xenodontinae), from Brazil. The new species differs from all other members of Proteocephalus by possessing a swollen elongated posterior part of the scolex herein considered as a metascolex. Furthermore, it is the only member of New World Proteocephalus possessing a voluminous glandular apical organ larger than suckers. P. joanae is also characterized by very elongated gravid proglottides. This is the first member of the Proteocephalidea occurring in Xenodon. Even though the species differs significantly from other species of the genus Proteocephalus, which currently contains many species that are morphologically very distinctive, it seems prudent to refrain from reworking the classification of the group until accurate redescriptions of Neotropical species can be conducted, preferably based on examination of type and freshly collected material. The definition of the metascolex is discussed herein.
Amazotaenia yvettae gen. n. and sp. n. (Proteocephalidea, Monticelliidae. Peltidocotylinae) is described from the intestine of the black-backed filhote, Brachyplatystoma filamentosum and from the piramutaba, B. vaillanti (Siluriformes: Pimelodidae) from Itacoatiara, Amazonia State, Brazil. The new genus differs from all other members of Peltidocotylinae in the morphology of the scolex, position of the vitelline follicles grouped in two elongated patches in the equatorial part of the proglottis, a smaller size of the strobila (less than 3 mm), smaller number of proglottides and smaller number of testes. The equatorial position of vitelline follicles, their shape in two elongated patches, the uterine development in Amazotaenia yvettae as well as the unusual behaviour of attachment in which individuals are grouped in compact clumps are peculiar within the Proteocephalidea. A key to the genera of the subfamily Peltidocotylinae is proposed. The sampling and processing methodology is also described in detail.