Three new genera of trypanorhynch cestodes from Australian elasmobranch fishes

Three new genera of trypanorhynch cestodes from Australian elasmobranch fishes collected in the Arafura Sea, off the Northern Territory, are described. Fossobothrium perplexum n. g., n. sp. (Otobothriidae), from the spiral valves of Anoxypristis cuspidata (Latham) and Pristis zijsron Bleeker, is similar to the otobothriid genera Pseudotobothrium Dollfus, 1942 and Poecilancistrium Dollfus, 1929 in possessing bothrial pits and a band of hooks on the tentacle, but differs from all known otobothriid genera in having the pits joined by a prominent velum. Iobothrium elegans n. g., n. sp. (Otobothriidae), from the spiral valve of Himantura jenkinsi (Annandale), is placed in the Otobothriidae because it possesses bothrial pits, but differs from Otobothrium Linton, 1890 and other genera in lacking intercalary hooks between the principal rows and in possessing a chainette on the external surface of the tentacle in the metabasal region. Oncomegoides celatus n. g., n. sp. (Eutetrarhynchidae), from the spiral valve of Dasyatis microps (Annandale) and Himantura jenkinsi, resembles Oncomegas Dollfus, 1929 in possessing two bothria and a megahook on the bothrial surface of the basal armature, but differs in possessing an extra row consisting of four intercalary hooks formed by the overlapping of two intercalary hooks on the external tentacular surface between each of the opposing principal rows and is therefore an atypical heteroacanth.     

An alternative classification of trypanorhynch cestodes considering the tentacular armature as being of limited importance

Based on a light- and scanning electron microscopical study of scolex morphology, tentacles and surface structures of 31 trypanorhynch species, an alternative classification of the trypanorhynch cestodes, adults, plerocerci and postlarvae, is presented. The arrangement of the tentacular armature is no longer used as a distinguishing feature for four different superfamilies. Instead, the presence or absence of ciliated pits and prebulbular organs is used to define three superfamilies: Tentacularioidea Poche, 1926; Otobothrioidea Dollfus, 1942; and Eutetrarhynchoidea Guiart, 1927. A total of 12 families are defined by the characters: the presence/absence of blastocysts, the number of bothridia and the reduction of the rhyncheal apparatus, together with a new character, complete rows of tentacular hooks (homeoacanth and heteroacanth typica) versus rows of hooks partly reduced (heteroacanth atypica and poeciloacanth). Of the 19 families previously accepted, 10 are retained (Eutetrarhynchidae, Gilquiniidae, Lacistorhynchidae, Mixodigmatidae, Otobothriidae, Paranybeliniidae, Pterobothriidae, Shirleyrhynchidae, Sphyriocephalidae and Tentaculariidae, all sensu nov.); one family is reinstated (i.e. Aporhynchidae Poche, 1926 sensu nov.) and a new one is added (i.e. Pseudotobothriidae n. fam.). Advantages of this alternative classification of trypanorhynch cestodes are: (i) the resolution of incongruities and questions caused by the use of the tentacular armature to distinguish superfamilies; (ii) the criteria for the establishment of higher taxa, superfamilies and families are clearly defined; (iii) with the findings of new species with different character combinations, this system can be enlarged up to 4 superfamilies and 48 families without loosing its stability; and (iv) all existing genera are easily re-assigned to the superfamilies and families.     

Some trypanorhynch cestodes from Hawaiian fishes, with descriptions of four new species.

Examination of teleost and elasmobranch fishes for cestodes from the Pacific Ocean off the Hawaiian Islands resulted in the recovery of 7 species of trypanorhynchs, 4 of which are new. The new species are Pseudogrillotia basipunctata, Pterobothrium hawaiiensis, Prochristianella micracantha, and Nybelinia basimegacantha. Tentacularia coryphaena Bosc 1797, Dasyrhynchus giganteus (Diesing 1859), and Parachristianella monomegacantha Kruse 1959 represent new host and distribution records. The family Pseudogrillotidae Dollfus 1969 is emended.     

Chimaerarhynchus n. g. andPatellobothrium n. g., two new genera of trypanorhynch cestodes with unique poeciloacanthous armatures,and a reorganisation of the poeciloacanthous trypanorhynch families

Chimaerarhynchus rougetae n. g., n. sp. is described fromSqualus acanthias andCentrophorus sp. from the coast of Senegal, and differs from all other trypanorhynch genera in having a chainette composed of dissimilar elements, that is, double-winged hooks alternating with pairs of hooks each with a single lateral wing. The new genus is allocated to the Gymnorhynchidae Dollfus, 1935.Patellobothrium quinquecatenatum n.g., n. sp. is described from the spiral intestine ofSphyrna mokarran from Darwin, Northern Territory, Australia and plerocerci fromRachycentron canadus from Queensland, Australia. The genus is distinguished from all others in possessing five chainettes. It is allocated to the family Mustelicolidae Dollfus, 1969. The relationships of all genera of trypanorhynchs possessing chainettes are discussed, and they are divided into three groups: (1) Dasyrhynchidae Dollfus, 1935, Lacistorhynchidae Guiart, 1927, Mustelicolidae and Hornelliellidae Yamaguti, 1954 are considered closely related since all genera possess two bothridia, a hermaphroditic duct and have hollow hooks; (2) Gymnorhynchidae, amended to contain onlyGymnorhynchus Rudolphi, 1819 andChimaerarhynchus n.g., is distinct in possessing four bothridia, an accessory seminal vesicle and hollow hooks; (3) Mixodigmatidae Dailey & Vogelbein, 1982, amended to includeMixodigma Dailey & Vogelbein, 1982 andHalysiorhynchus Pintner, 1913 has four bothridia, lacks seminal vesicles and a hermaphroditic duct and has solid hooks.A new family Molicolidae n. fam. is erected forMolicola Dollfus, 1935 andStragulorhynchus Beveridge & Campbell, 1988. The new family has a poeciloacanthous armature, and is distinguished by possessing a band of hooks on the external surface of the tentacle, four sessile bothridia and an acessory seminal vesicle.Myrmillorhynchus Bilqees, 1980 is suppressed as a synonym ofPterobothrium Diesing, 1850.Neogymnorhynchus Bilquees & Shah, 1982, is suppressed as a synonym ofPterobothrium, with the type species,N. platycephali becoming a synonym ofP. heteracanthum Diesing, 1850.Eulacistorhynchus Subhapradha, 1957 is considered agenus inquirendum;Gymnorhynchus cymbiumi Chincholikar & Shinde, 1977 is also a synonym ofPterobothrium heteracanthum Diesing, 1850.     

Cetorhinicola n. g., Shirleyrhynchus n. g. and Stragulorhynchus n. g., three new genera of trypanorhynch cestodes from elasmobranchs in Australian waters

Three new genera of trypanorhynch cestodes are described from Australian elasmobranchs: Cetorhinicola acanthocapax n. g., n. sp. from Cetorhinus maximus (Gunner, 1765), with four bothridia joined by avelum, a typical heteroacanthous armature with the ends of the hook rows not meeting on the external surface, and enlarged hooks on the base of the tentacle; Shirleyrhynchus butlerae n. g., n. sp., from Dasyatis fluviorum Ogilby, 1908 and D. sephen (Forsskal, 1775), with four bothridia, typical heteroacanthous armature, enlarged basal hooks, testes in linear rows, and lacking seminal vesicles; Stragulorhynchus orectologi n. g., n. sp., from Orectolobus tentaculatus (Peters, 1864) (type-host), O. maculatus (Bonnaterre, 1788) and O. ornatus (de Vis, 1882), with four bothridia, poeciloacanthous armature, with a band of hooklets on the external surface of the tentacle, external seminal vesicle, hermaphroditic duct, accessory seminal vesicle and post-ovarian testes. None of the new genera is readily accommodated by the existing classification of the Trypanorhyncha: the first two genera are tentatively allocated to the Gilquiniidae and the last to the Gymnorhynchidae.     

Antigenic affinity of cestodes in the genus Taenia

Antigens of four species of the genus Taenia (T. ovis ovis, T. ovis krabbei, T. hydatigena and T. parenchimatosa) were studied by means of immunodiffusion reaction in agar gel with the use of hyperimmune sera. It has been established that extracts of the studied cestodes contain a great number of antigens, which during parenteral administration cause a synthesis of antibodies in rabbits. In homologous systems the number of recorded antigen-antibody complexes varied from 5 to 10. The most close antigenic affinity was found between T. ovis ovis and T. ovis krabbei, T. ovis ovis and T. hydatigena, as far as the main mass of precipitation bands in the immunodiffusion reaction fused together that suggests the identity of corresponding antigenic components. In all cases when analysing antiserum to T. parenchimatosa extract no differences of species-specific character in heterologous systems were traced.     

Transberingian dispersal of cestodes in mammals

During Pleistocene glaciations, eustatic lowering of sea-level exposed the continental shelf between northeastern Eurasia and northwestern North America. That land in combination with unglaciated areas on the adjacent continents formed a vast region open to the west but bounded on the east by continental ice. Organisms from Eurasia spread into the unglaciated Beringian refugium, which was biotically an eastward extension of the Palaearctic. With rising sea-levels following glacial periods, the Bering Strait was formed and organisms of Eurasian origin were left within the nearctic sector of Beringia. As the continental ice disappeared, plants and animals spread eastward and southward from Beringia, while organisms from beyond the southern margins of the ice extended their ranges northward. The significance of Beringia is discussed with reference to the dispersal of host-specific cestodes in mammals that attained holarctic status during the late Pleistocene.     

Adenosine triphosphatases of cestodes Bothriocephalus scorpii

Activities and properties of adenosine triphosphatases (ATPases) have been studied in mitochondrial and microsomal fractions of cestodes Bothriocephalus scorpii parasitizing in pyloric appendages of the Brandt's bullhead Myoxocephalus brandti. The highest activity has been revealed in the mitochondrial fraction. The mitochondrial and microsomal fractions of B. scorpii have the ATPase activity dependent on the presence of cations Mg2+, Mn2+, and Ca2+. Effects of ions and inhibitors on the B. scorpii ATPase activity with various cations have been studied. Both subcellular fractions are able to hydrolyze, apart from ATP, also GTP, CTP, and UTP.     

Adenosine triphosphatases of cestodes Bothriocephalus scorpii

Activities and properties of adenosine triphosphatases (ATPases) were studied in mitochondrial and microsomal fractions of cestodes Bothriocephalus scorpii parasitizing in pyloric appendages of the Brandt’s bullhead Myoxocephalus brandti. The highest activity was revealed in the mitochondrial fraction. The mitochondrial and microsomal fractions of B. scorpii had the ATPase activity dependent on the presence of cations Mg²⁺, Mn²⁺, and Ca²⁺. Effects of ions and inhibitors on the B. scorpii ATPase activity with various cations were. Both subcellular fractions were able to hydrolyze, apart from ATP, also GTP, CTP, and UTP.     

Inactivation of proteolytic enzymes by cestodes

Inhibitor activity of cestodes from intestines of different hosts (sea birds, salt-water fish, and freshwater fish) was investigated. Alcataenia larina, Arctotaenia tetrabothrioides, Tetrabothrius erostris, T. minor, Wardium cirrosa, Bothriocephalus scorpii, Eubothrium rugosum, and Triaenophorus nodulosus were able to inhibit the activity of the commercial trypsin and activity of proteinase homogenates of the intestinal mucosa of the hosts. It was suggested that the inhibitor produced by the cestodes is specific for trypsin and protects them from the digestive enzymes of the host.     

Evolution of the trypanorhynch tapeworms: Parasite phylogeny supports independent lineages of sharks and rays

Trypanorhynch tapeworms (Platyhelminthes: Cestoda) are among the most diverse and abundant groups of metazoan parasites of elasmobranchs and are a ubiquitous part of the marine food webs that include these apex predators. Here we present a comprehensive analysis of their phylogeny, character evolution and host associations based on 10 years of sampling effort, including representatives of 12 of 15 and 44 of 66 currently recognized trypanorhynch families and genera, respectively. Using a combination of ssrDNA and lsrDNA (Domains 1-3) for 79 and 80 taxa, respectively, we maintain one-to-one correspondence between molecules and morphology by scoring 45 characters from the same specimens used for sequencing, and provide museum vouchers for this material. Host associations are examined through likelihood-based ancestral character state reconstructions (ACSRs) and by estimating dates of divergence using strict and relaxed molecular clock models in a Bayesian context. Maximum parsimony and Bayesian inference analyses of rDNA produced well-resolved and strongly supported trees in which the trypanorhynchs formed two primary lineages and were monophyletic with respect to the diphyllidean outgroup taxa. These lineages showed marked differences in their rates of divergence which in turn resulted in differing support and stability characteristics within the lineages. Mapping of morphological characters onto the tree resulting from combined analysis of rDNA showed most traits to be highly plastic, including some previously considered of key taxonomic importance such as underlying symmetries in tentacular armature. The resulting tree was found to be congruent with the most recent morphologically based superfamily designations in the order, providing support for four proposed superfamilies, but not for the Tentacularioidea and Eutetrarhynchoidea. ACSRs based on the combined analysis of rDNA estimated the original hosts of the two primary parasite lineages to be alternatively rajiform batoids and carcharhiniform sharks. This fundamental split provides independent support for rejecting the notion that rays are derived sharks, and thus supports the most recent molecular phylogenies of the Neoselachii. Beyond the basal split between shark- and ray-inhabiting lineages, no pattern was found to suggest that the trypanorhynchs have closely tracked the evolutionary histories of these host lineages, but instead, it appears that host-switching has been common and that the subsequent evolution of the parasites has been ecologically driven primarily through overlap in the niches of their shark and ray hosts. Using a relaxed molecular clock model calibrated by means of host fossil data, the ray-inhabiting lineage is estimated to have diversified around the Jurassic-Cretaceous boundary, whereas the shark-inhabiting lineage is estimated to have diversified later, in the Middle Cretaceous. Although the large error associated with the estimated divergence dates prevents robust conclusions from being drawn, the dates are nevertheless found to be consistent in a relative sense with the origins of their major hosts groups. The erection and definition of the suborders Trypanobatoida and Trypanoselachoida, for the major clades of trypanorhynchs parasitizing primarily rays and sharks, respectively, is proposed for the two primary lineages recovered here.     

Cestodes of cestodes of Peruvian freshwater stingrays

Adult tetraphyllidean tapeworms (Platyhelminthes: Eucestoda) from the spiral intestines of 3 species of potamotrygonid stingrays (Paratrygon aiereba, Potamotrygon castexi, and Portamotrygon motoro) in the Madre de Dios river in Peru were found to host numerous cysts embedded in their parenchymal tissues. Histological sections of the cysts revealed the presence of a scolex bearing 4 suckers and an unarmed apical organ consistent with larval stages of both Cyclophyllidea and Proteocephalidea. To further elucidate their identities, partial 28S ribosomal DNA (rDNA) sequences were characterized from 3 cysts and 4 adult Rhinebothrium spp. 'host' worms and screened against all available cestode 28S rDNA data. Initial BLAST screening and subsequent alignment ruled out the possibility that the cysts were cyclophyllidean, and the cyst and adult sequences were thus aligned together with all available lecanicephalidean, litobothriidean, proteocephalidean, and tetraphyllidean sequences. Sequences from all 3 cysts were identical, and phylogenetic analysis clearly placed them among derived members of the Proteocephalidea, although no exact match was found. Sequences from the adult host worms formed 2 identical pairs and grouped together with other tetraphyllidean species from rays. These results are compared with records of hyperparasites of South American catfish cestodes. This is the first confirmed record of a proteocephalidean cestode parasitizing a tetraphyllidean cestode.