The caudal bursa in the Heligmonellidae (Nematoda: Trichostrongylina). Characterization and hypothesis on its evolution.

The different patterns of the caudal bursa of the Heligmonellidae (Nematoda) are redefined, taking into account the grouping of rays 2-6 and the sequence of origin of these rays from their common trunk. The type of symmetry of the caudal bursa is also redefined. The following patterns were observed and characterized: the basic patterns: types 2-3, 2-2-1, 1-3-1 and 1-4 and the intermediary patterns: type 2-3 tending to type 2-2-1, type 2-2-1 tending to type 1-3-1, type 1-3-1 tending to type 1-4 and type 2-2-1 tending to type 1-4. An evolutionary interpretation of the patterns is attempted and seems to follow the direction: 2-3 to 2-2-1 to 1-3-1 to 1-4. Seven atypical patterns are described. The caudal bursae were classified based on their symmetry: subsymmetrical, dissymmetrical and asymmetrical. Independently of the type of symmetry, the two latero-ventral lobes may have the same or different patterns. The type of symmetry, the ratio between the two latero-ventral lobes and a characteristic pattern were utilized to characterize the caudal bursae at the level of the genus and the subfamily. The combination of the right/left ratio and the type of symmetry gives heterogeneous results, with no real association between these characters. The most conspicuous asymmetries and dissymmetries were found among the Nippostrongylinae. The most frequent pattern in the Heligmonellidae is the basic type 2-2-1; types 1-3-1 and 1-4 are less frequent but are characteristic of several genera; type 1-4 is absent from the Heligmonellinae. Whatever the pattern, in the Heligmonellidae rays 4 and 5 are the last to diverge from the common trunk of rays 2-6.

Redescription of Heligmosomoides neopolygyrus, Asakawa and Ohbayashi, 1986 (Nematoda: Heligmosomidae) from a Chinese rodent, Apodemus peninsulae (Rodentia: Muridae); with comments on Heligmosomoides polygyrus polygyrus (Dujardin, 1845) and related species in China and Japan.

Heligmosomoides neopolygyrus, Asakawa and Ohbayashi, 1986 (Nematoda, Heligmosomoidea) is redescribed from Apodemus peninsulae from Rangtang, Sichuan, China. A morphological review of the Heligmosomoides spp. belonging to the "polygyrus line" proposed by Asakawa (1988) is made using new characters. This enabled us to distinguish two subspecies in Mus musculus (Heligmosomoides polygyrus bakeri from Japan and H. p. polygyrus from China) and two valid species in Apodemus spp. (H. neopolygyrus from Japan (in A. peninsulae) and from China (in A. agrarius) and H. asakawae from China (in A. uralensis)). Three parasite species of A. agrarius and A. peninsulae, previously identified by Asakawa et al. (1993) as H. neopolygyrus, are considered to be Heligmosomoides incertae sedis. This is the first report of H. neopolygyrus in A. peninsulae from China.

Additional morphometrical data on some Heligmonellidae (Nematoda: Trichostrongylina) parasitic in Neotropical rodents (Cricetidae).

Some additional morphological and metrical data are provided, particularly on the synlophe of the following species: Hassalstrongylus dessetae Pinto, 1978, Stilestrongylus eta (Travassos, 1937), Stilestrongylus manni Denké & Murúa, 1977 and Stilestrongylus valdivianus Durette-Desset & Murúa, 1979, based on type and voucher material deposited in Brazilian and French collections. Heligmonoides crassidorsualis Franco, 1967 is considered as a Nippostrongylinae incertae sedis: its synlophe not being known it is impossible to report the species to a given genus. However, it is unlikely that the species belong to the genus Heligmonoides Baylis, 1928, present only in commensal Murinae from the Old World. Heligmonoides mirzai Smales, 2009, is also regarded, temporarily, as a Nippostrongylinae incertae sedis.

Description of a new species of Heligmosomoides (Nematoda: Heligmosomidae) parasitic in Microtus limnophius (Rodentia: Cricetidae) from Rangtang, Sichuan, China.

Heligmosomoides craigi n. sp. (Nematoda: Heligmosomoidea) is described from Microtus limnophilus Büchner, 1889 (Rodentia: Cricetidae) from Rangtang, Sichuan, China. It is related to H. protobullosus Asakawa, 1987 and H. longispiculum Tokobaev & Erkulov, 1966 both parasites of Microtus spp. from Japan and USSR, respectively by the following features: a ratio of spicule length/body length of more than 45% and rays 9 shorter than rays 10. The new species is differentiated by rays 8 being closed to rays 6 and 19-22 cuticular ridges versus 14 in H. protobullosus (synlophe not described in H. longispiculum). H. longicirratus (Schulz, 1954) also a parasite of Microtus sp. from the USSR is the most closely related species based on the number of cuticular ridges (20) and the ratio of spicule length/body length (48% versus 50%). There are no illustrations of this species and the female has not been described; for that reason, it is not possible to compare it accurately with our specimens.

Description of two new species of Nippostrongylinae (Nematoda: Heligmonellidae) coparasites in three sympatric species of Mastomys spp. (Rodentia: Muridae) from Senegal.

Two new species of heligmosomoid Trichostrongylina nematodes belonging to the genera Neoheligmonella Durette-Desset, 1970 and Heligmonina Baylis, 1928 are described. They are parasitic in the small intestine of three species of Mastomys from Senegal living in sympatry: M. natalensis (Smith, 1834), M. erythroleucus (Temminck, 1853) and M. huberti (Wroughton, 1909). Neoheligmonella granjoni n. sp. is closely related to three species from Senegal. They concern: N. bai Diouf & Durette-Desset, 2002 and N. dielmensis Diouf, Bâ & Durette-Desset, 1998, both parasitic in Arvicanthis niloticus Geoffroy, 1903 and N. mastomysi Diouf et al., 1998, a parasite of M. erythroleucus. N. granjoni n. sp. differs from these species by having 15 cuticular ridges at mid-body versus 13, a large carene and spicules taking up 10-15% of body length versus 5.3-7.1%. Heligmonina kanei n. sp. differs from the most related species H. kotoensis Diouf, Daouda & Durette-Desset 2005, a parasite of M. natalensis from Benin in the following features: spicules taking up 11.6% of body length on average versus 16.8%; a female tail three times longer than the distance anus-vulva versus a tail of equivalent size to this distance. In N. granjoni n. sp., where the material is abundant in all three hosts, the infra-specific variations observed (morphological or morphometrical) were not related to the host species. This is the first report of the genera Neoheligmonella and Heligmonina in M. huberti. The relevance of the phenomenon of host capture concerning the evolution of these two genera is confirmed.

Trichostrongylina (Nematoda) parasitic in Phyllotis sp. (Rodentia: Sigmodontinae) from Argentina, with description of three new species.

The Trichostrongylina parasitic in the leaf-eared mouse Phyllotis sp. (Sigmodontinae) from the Province of Catamarca, Argentina are studied. Three new species of Stilestrongylus Freitas, Lent and Almeida, 1937 (Heligmosomoidea: Heligmonellidae: Nippostrongylinae) are described. Stilestrongylus andalgala n. sp. is distinguished from the most closely related species S. moreli Diaw, 1976 parasitic in Auliscomys boliviensis from Bolivia, by the absence of a common trunk of right rays 2 and 3, by left ray 4 shorter than ray 5, and by the shape of the female tail, without a mucron. Stilestrongylus catamarca n. sp. is distinguished from all the other species in the genus by hypertrophied rays 2, larger than rays 3, and from the closely related species Stilestrongylus barusi Durette-Desset, 1971, parasitic in Sigmodontomys alfari from Colombia, by right ray 4 longer than ray 5 and left ray 4 shorter than ray 5, by a larger spicule length/body length ratio (22.6% vs. 7.2%), and by the presence of a mucron on the female tail. Stilestrongylus gracielae n. sp. most closely resembles Stilestrongylus azarai Durette-Desset and Sutton, 1985, parasitic in Akodon azarae and in Graomys griseoflavus, and Stilestrongylus franciscanus Digiani and Durette-Desset, 2003, also parasitic in G. griseoflavus, both from Argentina. These latter differ from the new species by the right lobe of the caudal bursa: in S. azarai rays 4, 5 and 6 arise at same level from their common trunk and in S. franciscanus right rays 4 and 5 diverge at their distal extremity. Lamanema chavezi Becklund, 1963 (Molineoidea: Molineinae), a parasite of South American camelids, is reported in rodents for the second time.

Do lagomorphs play a relay role in the evolution of the Trichostrongyuna nematodes?

In order to confirm or refute the relay role of lagomorphs in the evolution of the Trichostrongylina (Nematoda), the following points were studied by summarizing previous works on the subject: the chronology of the life cycles (27 conducted in natural hosts, lagomorphs, ruminants or arvicolin rodents; 14 in experimental hosts); the parasitic phase in the experimental host and the adaptation involved; the migration of the parasites into the tissues of the host; the morphogenesis of larval stages and molecular phylogeny. These data confirm, in their entirety, that lagomorphs may be considered as "relay" hosts in the evolution of the Trichostrongylina.

Trichostrongylina (Nematoda) from Malagasy Muridae. III--description of a new species of Heligmonoides Baylis, 1928 (Heligmonellidae) parasitic in Mus musculus.

Heligmonoides variabilis n. sp. (Heligmosomoidea, Nippostrongylinae) a parasite of Mus musculus from Madagascar is related to H. afghanus (Tenora, 1969), H. ikeharai Hasegawa, 1990 and H. josephi (Wertheim & Durette-Desset, 1976), all having the dorsal ray divided anterior to the arising of rays 8. H. ikeharai a parasite of Tokudaia muenninki (Muridae) from Japan is the most closely related species with rays 8 arising at mid-length along the dorsal ray. It is differentiated from the new species by very long spicules (almost half of body length) and by the length of the vestibule (almost one millimeter). A new definition of the genus Heligmonoides Baylis, 1928 is proposed with a dichotomic key of the species. The biogeographic distribution and the host spectrum of the genus are described.

A new species of Hypocristata (Nematoda, Trichostrongyuna, Heligmosomoidea) a parasite of Sigmodon hispidus (Cricetidae, Sigmodontinae) from Venezuela.

Description of Hypocristata tercera n. sp. (Heligmonellidae, Nippostrongylinae) a parasite of the small intestine of Sigmodon hispidus (Rodent, Sigmodontinae) from Venezuela. Two other species were described in the genus, both from Colombia and parasitic in Sigmodontinae. H. thomosomysi Durette-Desset, 1970, a parasite of Thomasomys sp. has about the same number of cuticular ridges at mid-body but differs by ridges having chitinoid struts, a caudal bursa pattern of type 2-2-1 (vs 1-3-1). H. anguillula Durette-Desset, 1970, a parasite of Sigmodontomys alfari (= Nectomys alfari) has the same caudal bursa pattern (type 1-3-1) but differs by the presence of ridges at mid-body in both sexes (absent at that level in H. tercera) and by ridges having chitinoid struts in female. This is the first report of the genus Hypocristata Durette-Desset, 1971 in Venezuela and in the genus Sigmodon (Sigmodontinae).

Three new species of the genus Oswaldocruzia Travassos, 1917 (Nematoda, Trichostrongylina, Molineoidea) parasites of Enyalius spp. (Iguanidae) from Brazil.

Three new species of the genus Oswaldocruzia Travassos, 1917 belonging to the sub-family Molineinae are described from the stomach and/or the small intestine of Enyalius spp. from Brazil. They belong to group 6 of Ben Slimane, Chabaud & Durette-Desset (1996). In this group they share along with O. peruensis Ben Slimane, Verhaag & Durette-Desset, 1995, a parasite of Iguanidae from Peru the followings linked characters: (i) a caudal bursa of type II; (ii) cervical alae present; (iii) undulated cuticular ridges. The Peruvian species differs from the Brasilian species by the absence of a strut in the cervical alae, by a small number of cuticular ridges at mid-body and by a spicular fork with a ramified inner twig. Oswaldocruzio fredi n. sp., a parasite of the stomach and the small intestine of Enyalius iheringii, mainly differs from the two other species by the absence of the oesophageal ventral cuticular ridges. Oswaldocruzia benslimanei n. sp., a parasite of the small intestine of Enyalius bilineatus, differs from Oswoldocruzia burseyi n. sp., a parasite of the stomach of Enyalius perditus, by the division of the fork at 23.4 % of spicule length (versus 32 %), and the length of the blade longer than the fork. Oswoldocruzia subauricularis sensu Freitas, 1955 nec Rudolphi, 1819 and O. mazzai sensu Vicente, 1981 nec Travassos, 1935 should be considered as species inquirendae.

The systematic position of some Ethiopian Nippostrongylinae (Nematoda, Trichostrongylina, Heligmosomoidea) from the National Collection of Animal Helminths, Onderstepoort, South Africa.

The taxonomic status of some nippostrongyline nematodes deposited in the National Collection of Animal Helminths, Onderstepoort, is revised. Heligmonina boomkeri n. sp. is described from Aethomys chrysophilus from South Africa. The most closely related species by the body measurements and the pattern of the caudal bursa is Heligmonina bignonensis Diouf, Bâ & Durette-Desset, 1997, a parasite of Mastomys erythroleucus from Senegal. It differs from the new species mainly in the number of ventral cuticular ridges at mid-body (four versus five) and the left ala in the male is shorter than the body diameter. The systematic position of Heligmonina spira (Ortlepp, 1939) and Neoheligmonella capensis (Ortlepp, 1939) is confirmed here through their synlophe, which was not previously studied.

The axis of orientation of the synlophe in the Heligmosomoidea (Nematoda, Trichostrongylina): a new approach.

The definition of the axis of orientation of the synlophe is modified for the Heligmosomoidea so that one or two axes may be recognized. When two axes are present, their inclinations to the sagittal axis are different on the right and left sides, and we propose to name them right axis and left axis, respectively. During the course of evolution, starting from a single oblique axis (plesiomorphic state), an independent rotation of this axis on the right and left sides may bring about a double-axis state with a different inclination on both sides (derived state). When the rotation reaches 90 degrees for both sides, the axis becomes simple once again and is superimposed to the frontal axis (most derived state).

Comparative ultrastructure of the cuticle of trichostrongyle nematodes.

The ultrastructure of the cuticle was examined in Austrostrongylus victoriensis, Patricialina birdi and Woolleya monodelphis (Herpetostrongylidae) from marsupials, Paraustrostrongylus ratti (Herpetostrongylidae) from rodents, Nippostrongylus magnus and Odilia bainae (Heligmonellidae) from rodents, Cooperia oncophora and Camelostrongylus mentulatus (Trichostrongylidae) from ruminants, and Nematodirus spathiger (Molineidae) from ruminants. The principal cuticular layers described previously were present in all species investigated. Major differences in the shape and composition of cuticular struts were observed as well as differences in components of the median zone of the cuticle, including the fluid-filled regions present in several species. Several different types of strut were observed. Although strut structure within the Heligmonellidae appeared to be constant, there were variations within both the Herpetostrongylidae and Trichostrongylidae. In Nem. spathiger the cuticular ridges lacked struts. The diversity of structures found in the species examined suggests that more extensive comparative studies of the trichostrongyle cuticle are warranted.

A cladistic analysis of the genera in the subfamily Pudicinae (Nematoda, Trichostrongyloidea, Heligmonellidae).

A parsimony analysis was performed on 37 specific taxa belonging to the subfamily Pudicinae (family Heligmonellidae), which contains parasites mainly from South American caviomorph rodents. Thirteen characters were used from the synlophe (rotation of axis, presence of carene, carene asymmetry, presence of comaretes, single ventral comarete length, ridge discontinuity, ventral ridge numbers, presence of a peculiar posterior synlophe, presence of supernumerary spines) and the male caudal bursa (relative length of rays 9 and 10, caudal bursa type, division of the dorsal ray, divergence of the 10th rays). The cladogram shows a consistency index of 1.0. The subfamily Pudicinae has two synapomorphies. Two suprageneric groups are recognized. Suprageneric group 1 shows one synapomorphy and contains Heligmostrongylus, Fuellebornema, Sciurodendrium and Pseudoheligmosomum; suprageneric group 2 shows two synapomorphies and contains Pudica, Acanthostrongylus, Justinema and Durettestrongylus. Five genera are defined on the basis of synapomorphies. The genera Heligmostrongylus, Sciurodendrium and Pudica which are considered paraphyletic, however, are retained due to lack of knowledge as to their relationships.

The origins and evolutionary expansion of the Strongylida (Nematoda).

The Strongylida are thought to have arisen from free-living rhabditoid nematodes, but the relationships between the major groupings within the Strongylida, the Strongylina, the Metastrongylina, Trichostrongylina and the Ancylostomatina are far from clear in spite of the abundance of morphological data now available for analysis. Evolutionary mechanisms including co-evolution, host switching, host dispersal, use of intermediate hosts, various sites of localisation within the definitive host and modifications of life-cycle strategies appear to have been utilised in the expansion of the Strongylida, with different mechanisms predominating in different families or superfamilies. Co-evolution appears to have been a major mode of evolution in the Strongylina, in contrast to the Trichostrongylina, which have used host dispersal and host-switching to great advantage. The phylogeny of the Ancylostomatina shows little association with host evolution, but does match the feeding preferences of the hosts. The Metastrongylina have utilised intermediate hosts and life cycle modifications including a shift to extra-intestinal sites as major means of diversification, in contrast to the other sub-orders. The review, while indicating much progress in our understanding of the phylogeny of the Strongylida, also reveals that enormous gaps still exist, and emphasises the tentative nature of many of the phylogenetic hypotheses tendered to date.

Internal transcribed spacer rDNA can be used to infer the phylogenetic relationships of species within the genus Nematodirus (Nematoda: molineoidea).

Sequences of the first internal transcribed spacer rDNA were characterised for four veterinary important species of gastrointestinal nematodes from the genus Nematodirus. The sequence data were combined with previously published data of the second internal transcribed spacer to determine whether these rDNA regions provided a suitable number of informative characters to determine the phylogenetic relationships of species within the genus. A total of 32 alignment positions of the first internal transcribed spacer data set and 33 characters from the second internal transcribed spacer data set were informative in phylogenetic analyses. Irrespective of whether the data from each spacer were analysed separately or combined, only one most parsimonious tree was produced, with the relationships of the four species fully resolved. In addition, several regions of conservatism in the first internal transcribed spacer sequence among the four Nematodirus species suggests that this rDNA region may also provide phylogenetic information for higher taxonomic levels within the Molineoidea.

A cladistic analysis of the Trichostrongyloidea (Nematoda).

A morphologically based cladistic analysis of 40 genera included within the Trichostrongyloidea (Amidostomatidae, Dromaeostrongylidae and Trichostrongylidae) is proposed. Two genera were used as outgroups, one from the Strongylina and the other from the Ancylostomatina. Seven genera do not appear in the matrix because some significant morphological characters remain unknown for these genera. Nonetheless, except for Moguranema which is excluded as incertae sedis, a likely systematic position could be assigned to them based on the morphological characters that are known. The classification which best fits the consensus tree is composed of three families. In adding the genera not included in the tree, we obtain: (i) Trichostrongylidae with three sub-families, Amidostomatinae (four genera), Filarinematinae (three genera) and Trichostrongylinae (five genera); (ii) Haemonchidae with two sub-families: Ostertagiinae (eight genera) and Haemonchinae (five genera); (iii) Cooperiidae with three sub-families: Libyostrongylinae (five genera), Obeliscoidinae n. subfam. (five genera) and Cooperiinae (ten genera). Dromaeostrongylus and Ortleppstrongylus, whose females have a caudal spine, are excluded from the Trichostrongyloidea and are placed in the Molineoidea. The hypotheses relating to the evolutionary history of the Trichostrongyloidea are: the origin of the superfamily could have occurred during the upper Cretaceous period. The two most ancient sub-families (Amidostomatinae and Filarinematinae) would be of Gwondwanan origin and evolved during the Paleocene period within Neotropical aquatic birds and within the Australian marsupials. The Trichostrongylinae would have arisen during the Eocene period within birds and then adapted to diverse archaic mammals in the Neotropical region on one hand and in the Nearctic region, on the other hand and lastly adapted to the Lagomorpha and subsequently to the Ruminantia. In both families originating from the Trichostrongylidae, the adaptation to the Lagomorpha may have taken place during the Oligocene but in a different way. In the Haemonchidae, the Ostertagiinae may have passed directly from the Neartic region to Europe. In the Cooperiidae, the adaptation to Lagomorpha may have occurred either within the Libyostrongylinae which may have remained in the Ethiopian region since the Paleocene, or, more likely, by the passage of the Obeliscoidinae from the Nearctic region to the Asian, through the Bering strait. In all cases, the adaptation of the Trichostrongyloidea of Lagomorpha to Ruminants apparently took place during the Miocene, mainly in the Palearctic and the Ethiopian regions.

Intestinal migrations of Trichostrongylus retortaeformis (Trichostrongylina, Trichostrongylidae) in the rabbit.

Observations were made on histological sections of the stomach and small intestine of seven rabbits infected with Trichostrongylus retortaeformis and from one uninfected control rabbit. At 12h post-infection, larvae were found in the small intestine. At first, only a few larvae were observed entering the mucosa through capillaries of the stroma of villi; the majority of larvae remained in the intestinal lumen, within mucus of the crypts. We consider that the presence of the worms in the stroma is the result of a larval migration. From a phyletic point of view, this migration is interpreted as an ancestral memory of the pulmonary migration seen in the primitive Strongylida.

Description of Ostertagia ostertagi and Ostertagia leptospicularis hybrids in experimentally infected sheep.

Hybrids of Ostertagia ostertagi and Ostertagia leptospicularis, derived from experimental infections in sheep, are described. Morphometrics of the hybrids were intermediate between those of parental lines for a large range of parameters (distance from apex to cervical papillae and length of esophagus for males and females, length of spicules for males, and length of vestibule, distance from vulva to the end of tail, width of tail at anus). The morphological relationship between hybrids and their parent species was assessed by discriminant analysis based on the relative values of these parameters (actual value/length of the worm). Each parental line, either bred in sheep or in the natural host, was morphologically similar and differed from hybrids.

Helminths from introduced small mammals on Kerguelen, Crozet, and Amsterdam Islands (southern Indian Ocean).

Four monoxenous nematodes and 1 heteroxenous cestode were found in 4 species of introduced small mammals on isolated sub-Antarctic islands of the Indian Ocean. In the Kerguelen Archipelago, Syphacia obvelata, Passalurus ambiguus (Nematoda: Oxyuridae), and Rodentolepis straminea (Cestoda: Cyclophyllidae) were respectively found in the house mouse Mus musculus, the rabbit Oryctolagus cuniculus, and the black rat Rattus rattus. One accidental nematode, Trichostrongylus sp. (Nematoda: Trichostrongylidae), was also found in a black rat on Kerguelen. On Possession Island (Crozet Archipelago), R. straminea was present in the black rat. On Amsterdam Island, the brown rat R. norvegicus harbored 2 species, R. straminea and Nippostrongylus brasiliensis (Nematoda: Heligmonellidae). The small number of founder hosts and the depauperate terrestrial communities on these remote islands explain the low diversity in the helminth communities of these introduced mammals compared with continental populations.