Alain de Chambrier

Preliminary phylogenetic analysis of subfamilies of the Proteocephalidea (Eucestoda)

Cladistic analysis based on comparative morphology was used to examine the subfamily-level relationships within the cestode order Proteocephalidea. A single most parsimonious tree (70 steps, CI = 0.571; RC = 0.295; HI = 0.471) is consistent with monophyly for the Proteocephalidea and showed a relatively high consistency at the family level with the diagnosis of two major subclades. Unambiguous support for a Proteocephalidae subclade, including the Corallobothriinae, Proteocephalinae, Gangesiinae and Sandonellinae, and a Monticelliidae subclade, including the Marsypocephalinae, Zygobothriinae, Monticelliinae, Rudolphiellinae, Ephedrocephalinae and Othinoscolecinae was evident. Two subfamilies, the Acanthotaeniinae (historically in the Proteocephalidae) and Nupeliinae (historically in the Monticelliidae), were however, basal to all other subfamilies, indicating that neither family as currently conceived is monophyletic. Trees one or two steps longer, however, would be consistent with monophyly for the Proteocephalidae and Monticelliidae (excluding Acanthotaeniinae) or would result in the monophyly for both families, including all respective subfamilies congruent with current concepts for systematics of the order. Zoogeographical analysis demonstrated a strong Gondwanan association; proteocephalideans originated in Africa, with subsequent development linking Africa and South America. Colonisation of the Northern Hemisphere by proteocephalid subfamilies, the Proteocephalinae, Corallobothriinae and Gangesiinae, was secondary. Analysis of parasite-host relationships indicated that the basal hosts for the Proteocephalidea are equivocal; siluriform teleosts were, however, the basal hosts for the Nupeliinae + the Monticelliidae and Proteocephalidae subclades and an extensive co-evolutionary history with this host group is postulated. Independent colonisation events of reptilians by species of the Proteocephalinae and Acanthotaeniinae, non-siluriform teleosts associated with the Sandonellinae and some Proteocephalinae, and amphibians by some Proteocephalinae, are recognised. Some points which should be considered for further development of the systematics of the group are proposed, with special emphasis given to thorough morphological descriptions and investigations of life-cycles.

Révision des cestodes (Monticelliidae) décrits par Woodland (1934) chez Brachyplatystoma filamentosum avec redéfinition des genres Endorchis Woodland, 1934 et Nomimoscolex Woodland, 1934

In 1934, Woodland described three new species of proteocephalidean tapeworms (Monticelliidae) from the Amazonian siluriform fish Brachyplatystoma filamentosum: Endorchis piraeeba (type-species), Nomimoscolex piraeeba (type-species) and Amphoteromorphus piraeeba. Examination of Woodlands type-material and its comparison with newly collected specimens from the same host close to the type-localities revealed inaccuracies in Woodlands diagnoses of these taxa. The main problems concern the scolex of E. piraeeba, the gravid proglottis of N. piraeeba and aspects of the anatomy of A. piraeeba. In our revision, we establish that: (1) the scolex assigned by Woodland to E. piraeeba belongs to N. piraeeba, and the actual scolex of E. piraeeba is characterised by bi-lobed suckers; (2) the gravid proglottis figured by Woodland does not belong to N. piraeeba, differing in particular, in the presence of paramuscular vitelline follicles and the cirrus-pouch length/proglottis width ratio; and (3) the cross-section assigned by Woodland to A. piraeeba belongs to N. piraeeba.This study enabled the redescription of all three taxa and the presentation of new diagnoses for the genera Nomimoscolex and Endorchis. The latter genus is considered valid. A lectotype is designated for N. piraeeba. In addition, members of the genus Nomimoscolex were revised and seven of 16 species were transferred to other genera or considered to be species inquirendae. N. magna Rego, Santos & Silva, 1974 becomes, in part, Monticellia magna n. comb. and, in part, Proteocephalus sp. N. piracatinga Woodland, 1935 becomes M. amazonica nom. nov. (to avoid homonyny with M. piracatinga Woodland, 1935). Proteocephalus chubbi Pavanelli & Takemoto, 1995 becomes N. chubbi (Pavanelli & Takemoto, 1995) n. comb. N. pirarara (Woodland, 1935) becomes P. pirarara n. comb. and N. woodlandi (Rego, 1984) becomes P. hemioliopteri nom. nov. (to avoid homonymy with P. woodlandi Moghe, 1926). N. pimelodi Gil de Pertierra, 1995 becomes P. pimelodi n. comb. nov. N. arandasregoi is considered a species inquirendae. N. alovarius is not classified. N. dorad is considered a synonym of N. piraeeba. In the light of recent ultrastructural data, the spines on N. piraeeba are considered as true microtriches. The following species are considered members of the genus Nomimoscolex: N. admonticellia, N. chubbi, N. lenha, N. lopesi, N. matogrossensis, N. microacetabula, N. piraeeba, N. sudobim and N. touzeti.A. peniculus Diesing of Woodland (1933) is considered conspecific with Amphoteromorphus piraeeba Woodland, 1934.In this study, we point out the importance of careful comparative morphological studies and taxonomic work. In the present case, the revision of the original material, without the study of new specimens, would have been inadequate to accurately define specific structural attributes as the basis for allocation of species at the generic level.

Nomimoscolex suspectus n. sp. (Eucestoda: Proteocephalidea: Zygobothriinae) with morphological and molecular phylogenetic analyses of the genus.

We describe a new species of Nomimoscolex from the Amazon siluriform fishes Brachyplatystoma filamentosum, B. flavicans and B. vaillanti. It differs from N. piraeeba in a lower mean number of testes, the paramuscular position of the vitelline follicles, the ovarian width/proglottis width ratio and the cirrus-pouch length/proglottis width ratio. Protein electrophoresis assays performed for 25 enzymatic systems showed that specimens of N. suspectus n. sp. from the three host species form a homogenous population which was genetically isolated from N. piraeeba and N. dorad. Moreover, the latter two species, synonymised by Rego (1991) because of their close morphological similarity, could be separated at eight loci. We thus restore N. dorad as a valid species. We finally examined the composition of the genus Nomimoscolex using DNA sequences from the 5.8S rRNA, ITS-2 and 28S rRNA nuclear ribosomal genes and a matrix of 24 morphological characters. Phylogenetic relationships were inferred for nine species of the genus, five members of other monticelliid genera and two outgroup species. The results of the phylogenetic analyses performed on morphological and molecular characters converged with those from allozyme studies and showed that N. suspectus, N. piraeeba and N. dorad clustered in a distinct clade that excluded other members of the genus. We therefore recognised them as an aggregate of species to reflect an isolation supported by both morphological and genetic data. Because relationships among the remaining Nomimoscolex representatives and other genera were generally poorly resolved, regardless of the database analysed, no action was taken to reorganise them into alternative groupings.

Tapeworms (Cestoda: Proteocephalidea) of Fishes from the Amazon River in Peru

Abstract This article provides the first data on the occurrence of adult proteocephalidean tapeworms (Cestoda) in freshwater fishes from the Peruvian part of the Amazon River. In total, 29 species of proteocephalidean cestodes of the genera Amphoteromorphus, Chambriella, Choanoscolex, Euzetiella, Houssayela, Mariauxiella, Monticellia, Nomimoscolex, Nupelia, Peltidocotyle, Proteocephalus, Rudolphiella, Scholzia, Sciadocephalus, Spatulifer, Travassiella, and Zygobothrium are reported from 10 species of pimelodid, heptapterid and doradid catfish and the cichlids Astronotus ocellatus and Cichla monoculus. All species are reported from western Amazonia and Peru for the first time, with 6 taxa representing new geographical records for the Amazon River basin. The most remarkable finding is that of Houssayela sudobim (Woodland, 1935) from Pseudoplatystoma fasciatus, reported for the first time since its original description. Four other taxa (Chambriella sp. and Proteocephalus sp. from Phractocephalus hemioliopterus, Nupelia sp. from Goeldiella eques, and Proteocephalus sp. from Pterodoras granulosus) may be new for science. A list of the species found is provided together with brief comments on their fish hosts and geographical distribution. In addition to adult tapeworms, larvae (metacestodes) of proteocephalideans were found encysted in the mesenteries, intestinal wall, and gills of small catfish.

Etude morpho-anatomique et génétique de deux nouveaux Proteocephalus Weinland, 1858 (Cestoda: Proteocephalidae) parasites de Platydoras costatus (L.), poisson siluriforme du Paraguay

The cat-fish Platydoras costatus (L.) is abundantly parasitised by the cestode genus Proteocephalus in Paraguay, previously unrecorded from this host. Morpho-metrical studies suggest the presence of two species, Proteocephalus soniae n. sp. and P. renaudi n. sp. They differ in the scolex, the distribution of the testes, the mean number of testes and uterine diverticula, the presence or absence of a vaginal sphincter, and the shape of the eggs and their envelopes. A single specimen, representing a possible third taxon, is morphologically similar to P. renaudi. Data from protein electrophoresis on amidon gel confirm the morpho-metrical conclusions. Of the 13 enzymes investigated, ACP, AAT, GPI and MDH have alleles of different electrophoretic mobilities in the three taxa. Only two alleles are distinguishable on locus HK. There is no evidence of heterozygotes in the tested systems. The specific status of the examined taxa is therefore confirmed. More material of the third species is required for establishing a species definition. P. renaudi has following unique anatomical features: the egg bears an enormous external envelope and an elongate embryophore with a unilateral appendix; the vitelline glands are paramuscular; and the eggs, laid in packets, are evacuated in an unusual way.The establishment of species based on protein electrophoresis allows a critical examination of the validity of anatomical characters usually used for taxonomic purpose. Good specific characters are the presence or absence of an apical organ and a vaginal sphincter and the relatively constant ratio between ovary width and the width of mature proglottids. The number of testes and uterine diverticula, both frequently used in species diagnoses, show variations which are often considerable and are, therefore, less unequivocal. The coefficients of variation observed calculating the mean numbers of testes can be high and reach up to 28%. This variation is itself a specific character in our opinion.

A New Genus and Species of Proteocephalidean (Cestoda) From Clarias Catfishes (Siluriformes: Clariidae) in Africa

Abstract A new proteocephalidean cestode is described from 2 catfishes, Clarias gariepinus (type host) and C. cf. anguillaris (Siluriformes: Clariidae), from Ethiopia (type locality), Sudan, Tanzania, and Zimbabwe, and a new genus, Barsonella, is proposed to accommodate it. The genus belongs to the Proteocephalinae because its genital organs (testes, ovary, vitellarium, and uterus) are situated in the medulla. Barsonella lafoni, the type and only species of the new genus, is characterized mainly by the possession of an additional opening of each sucker; circular musculature on the anterior margin of suckers, serving as a sphincter; a small thin-walled glandular apical organ; absence of well-developed osmoregulatory canals in mature, pregravid, and gravid proglottids; and a large strobila, up to 173 mm long and 3.2 mm wide. Species of Marsypocephalus Wedl, 1861 (Marsypocephalinae), other large-sized proteocephalidean tapeworms occurring sympatrically in African catfishes (Clarias and Heterobranchus) and also possessing a sphincter-like, circular musculature on the anterior part of suckers, differ from B. lafoni in the absence of an additional sucker opening and glandular apical organ, the cortical position of the testes, well-developed osmoregulatory canals throughout the strobila, and a large cirrus sac. Proteocephalus glanduligerus (Janicki, 1928), another cestode parasitic in Clarias spp. in Africa, is much smaller than B. lafoni (maximum length 15 mm), has suckers without additional opening and circular musculature on the suckers, a large-sized glandular organ, much larger than suckers, and well-developed osmoregulatory canals. Comparison of partial sequences of the 28S rRNA gene for 7 samples of B. lafoni from 2 different hosts and 4 localities in Ethiopia, Sudan, and Tanzania has shown a very low genetic variability. In a limited phylogenetic analysis, B. lafoni formed a clade with Corallobothrium solidum Fritsch, 1886 (Proteocephalidae: Corallobothriinae), an African electric catfish parasite. This clade was the sister group of almost all Neotropical taxa from pimelodid and other catfishes.

Nomimoscolex pertierrae n. sp. (Eucestoda: Proteocephalidea), a parasite of Pseudoplatystoma corruscans (Siluriformes: Pimelodidae) in Brazil and redescription of N. sudobim Woodland, 1935, a parasite of P. fasciatum

The cestode Nomimoscolex sudobim Woodland, 1935 (Proteocephalidea) is redescribed on the basis of its type-specimens and recently collected material found in the intestine of the ‘sudobim’ Pseudoplatystoma fasciatum (Siluriformes: Pimelodidae) (type-host), from the Amazon River (near the type-locality). Nomimoscolex pertierrae n. sp. is described from the ‘surubi’ Pseudoplatystoma corruscans from the Paraná River around Porto Rico. Among fifteen known Nomimoscolex species, only N. sudobim possess a cortical uterus in combination with osmoregulatory canals some distance internal to the proglottis margins, as in N. pertierrae n. sp. N. pertierrae differs from N. sudobim, which exhibits the most similarity with the former species, in the morphology of the scolex, the size and unusual shape of microtriches (slender digitiform) on the internal and marginal regions of the suckers, and in the lower mean number of testes [(114 in N.␣pertierrae, ranging between 216 (recently collected material) and 240 (type-material) in N. sudobim)]. The material described as N. sudobim by Pavanelli & Rego (1992) from the intestine of P. corruscans is considered to be N. pertierrae. The utility of microtriches as characters for distinguishing between species is demonstrated in the clear differences in the shape of those of N. pertierrae and N. sudobim. The morphology of microtriches warrants more attention in future studies on the taxonomy of proteocephalidean cestodes.

Mariauxiella pimelodi n. g., n. sp. (Cestoda: Monticelliidae): a parasite of pimelodid siluroid fishes from South America

Mariauxiella pimelodi n. g., n. sp. (Cestoda, Monticelliidae, Othinoscolecinae) is described from the South American siluriform fishes Pimelodus ornatus and Pimelodus sp. caught in Brazil and Paraguay. When compared with other genera of South American monticelliids, the new genus exhibits the following morpho-anatomical characters: the particular development of the distal circular musculature of the suckers acting as a sphincter; the medullar ovary projecting numerous lobules into the dorsal cortex; and the uterus situated in the ventral cortex but with numerous outgrowths penetrating the medulla and reaching the dorsal cortex in pregravid proglottids. The new species is the fourth monticelliid cestode recorded from Pimelodus.

Thaumasioscolex didelphidis N. Gen., N. Sp. (Eucestoda: Proteocephalidae) from the Black-Eared Opossum Didelphis marsupialis from Mexico, the First Proteocephalidean Tapeworm from a Mammal

Thaumasioscolex didelphidis n. gen., n. sp. is described from the intestine of the black-eared opossum Didelphis marsupialis L. (Marsupialia: Didelphidae) from Los Tuxtlas, Veracruz, Mexico. The new genus differs from all proteocephalidean genera in the morphology of the scolex that is formed by 4 well separated lobes each containing 1 noncircular sucker opening laterally inside the exterolateral cavity, a large-sized body (length up to 1 m), a large number of testes, the shape of gravid proglottids that are inversely craspedote (the anterior border of a proglottid overlaps the posterior border of a preceding proglottid), eggs in groups mostly of 4–6 eggs each, and an embryophore bearing digitiform projections on its external surface. This is the first tapeworm of the Proteocephalidea, the members of which were previously reported exclusively from poikilotherm vertebrates (freshwater fishes, amphibians, and reptiles), found in a homoiotherm vertebrate.

SANDONELLA SANDONI (LYNSDALE, 1960), AN ENIGMATIC AND MORPHOLOGICALLY UNIQUE CESTODE PARASITIC IN THE OSTEOGLOSSIFORM FISH HETEROTIS NILOTICUS IN AFRICA

Sandonella sandoni (Lynsdale, 1960) is the type and only species of the Sandonellinae, a cestode subfamily of unclear phylogenetic position. It is redescribed here on the basis of a re-examination of its syntypes, voucher specimens from museum collections, and freshly collected material from the intestine of Heterotis niloticus (Osteoglossiformes: Arapaimidae) from Benin, Nigeria, Senegal, and the Sudan. The species possesses several unique morphological characters, such as (1) a vitellarium formed by 2 compact, but deeply lobulated, postovarian masses near the posterior margin of proglottids; (2) a scolex with a highly modified apical structure formed by 4 muscular retractile lappets; (3) a well-developed circular musculature, which is external to the inner longitudinal muscles; (4) a dilated, vesicle-like proximal part of the external sperm duct; (5) the unique morphology of the uterus and its development, which represents an intermediate form between the 2 basic types recognized in the Proteocephalidea; (6) the growth of eggs during their development within the uterus; and (7) the complex proglottization with intermingled smaller and larger (wider) proglottids. The morphology of S. sandoni, including the form and distribution of microtriches, was studied by scanning electron microscopy for the first time, and the lectotype and paralectotypes of S. sandoni are designated. Sequences of the 28S rRNA gene of 4 specimens (2 from the Sudan and 2 from Senegal) were identical, which confirms conspecificity of geographically distant samples. Sandonella sandoni sequences have also shown that it actually belongs among the Proteocephalidea, being a sister taxon of a relatively derived clade of Palaearctic proteocephalideans, containing Glanitaenia osculata and Paraproteocephalus parasiluri from catfish and Palaearctic species of the Proteocephalus aggregate.