A new cestode species Paranoplocephala gubanovi sp.n. (Cyclophyllidea: Anoplocephalidae) from the wood lemming Myopus schisticolor of eastern Siberia

A new species of anoplocephalid cestode, Paranoplocephala gubanovi sp. n. (Cyclophyllidea, Anoplocephalidae), from wood lemmings of Eastern Siberia (Myopus schisticolor) is described. The new species differs from other known species of Paranoplocephala associated with Holarctic lemmings by having unique combination of characters as follows: a few-segmented strobila, superficial suckers sticking out of the scolex, ovary covering practically the whole middle part of the segment, relatively little number of testicles situated in the aporal part of the segment, cirrus bursa crossing the poral excretory vessels, and subspherical spermatheca situated in the middle part of the segment. Comparison of P. gubanovi sp. n. and several closest species, P. fellmani Haukisaimi et Henttonen, 2001, P. serrata Haukisaimi et Henttonen, 2000, and P. arctica (Rausch, 1952) has been carried out. Features distinguishing the new species from Aprostatandrya macrocephala and A. microti have also been studied.     

Molecular and morphological evidence for multiple species within Paranoplocephala omphalodes (Cestoda, Anoplocephalidae) in Microtus voles (Arvicolinae)

Haukisalmi, V., Wickström, L. M., Henttonen, H., Hantula, J. & Gubányi, A. (2004). Molecular and morphological evidence for multiple species within Paranoplocephala omphalodes (Cestoda, Anoplocephalidae) in Microtus voles (Arvicolinae). —Zoologica Scripta, 33, 277–290. The present study was designed to test the hypothesis that the anoplocephalid cestode Paranoplocephala omphalodes (Hermann, 1783), a Holarctic parasite of Microtus voles, is a complex of host‐specific species, rather than a single host‐generalist species, using uni‐ and multivariate morphometrics and DNA sequence data from the mitochondrial cytochrome oxidase I gene. The phylogenetic methods applied to the mtDNA sequence data showed consistently that the cestodes morphologically recognizable as P. omphalodes include four well‐supported monophyletic groups, representing at least three distinct, largely host‐specific species. Multivariate morphometrics (discriminant analysis) successfully distinguished the four main mtDNA clades of P. omphalodes‐like cestodes. The true P. omphalodes is shown to be a parasite of Microtus arvalis, M. agrestis and Clethrionomys glareolus in Europe. Microtus oeconomus harbours two host‐specific, allopatric and possibly conspecific clades, one with a Holarctic and another with an (eastern) Beringian (Alaskan) distribution. The eastern Beringian endemic M. miurus is also parasitized with a host‐specific, morphologically divergent species of Paranoplocephala. The cestode clades recognized in M. oeconomus and M. miurus represent 2–3 undescribed species. Molecular phylogenetic analyses supported the monophyly of the ‘northern clade’ of Paranoplocephala spp., an assemblage including P. kalelai from Clethrionomys spp., P. macrocephala from Microtus spp. and all clades of P. omphalodes‐like cestodes except those representing the true P. omphalodes from Europe. The intra‐ and interspecific phylogeny within the northern clade is compared tentatively with the known evolutionary history of the hosts.     

Description of Paranoplocephala yoccozi n. sp. (Cestoda: Anoplocephalidae) from the snow vole Chionomys nivalis in France, with a review of anoplocephaud cestodes of snow voles in Europe

We describe Paranoplocephala yoccozi n. sp. (Cestoda: Anoplocephalidae) from the snow vole Chionomys nivalis in Bourg-Saint-Maurice, French Alps, compare it with several related species from rodents, and review the anoplocephalid cestodes of snow voles in Europe. Paranoplocephala yoccozi n. sp. is primarily distinguished from the related species by its large scolex of characteristic shape, robust neck region, and the structure of the cirrus sac, vitellarium and vagina. We show that the anoplocephalid cestodes of snow voles in Europe, representing the genera Anoplocephaloides and Paranoplocephala, include at least seven species. This fauna consists primarily of species that snow voles share with other voles inhabiting the high-mountain areas. Some of the species, including P. yoccozi n. sp., appear to have a very localized distribution, which is assumed to be a consequence of the historical fragmentation of snow vole populations.     

Paranoplocephala maseri n. sp. (Cestoda,Anoplocephalidae), a parasite of sagebrush voles Lemmiscus curtatus (Rodentia) in the USA

Paranoplocephala maseri n. sp. is described from Lemmiscus curtatus (Cope) in the USA. The new species is related to Paranoplocephala omphalodes (Hermann, 1783), P. caucasica (Kirschenblat, 1938), P. kirbyi Voge 1948, P. microti (Hansen, 1947) and P. macrocephala (Douthitt, 1915) sensu Genov et al. (1996). P. maseri n. sp. differs from P. omphalodes in the position of the genital pores, testes and cirrus-sac; from P. caucasica, in which there is an unarmed cirrus, in both the distribution and larger number of testes; from P. kirbyi in the distribution of the testes, the position of the genital pores and egg dimensions; from P. microti in the distribution and smaller number of testes, the smaller egg dimensions and the position of the genital pores; and from P. macrocephala in the position of genital pores and cirrus-sac.     

Biogeography of helminth parasitism in Lemmus Link (Arvicolinae), with the description of Paranoplocephala fellmani n. sp. (Cestoda: Anoplocephalidae) from the Norwegian lemming L. lemmus (Linnaeus)

We describe the gastrointestinal helminth fauna of true lemmings (Lemmus spp., Arvicolinae) based on published and original material throughout the Holarctic range of these hosts. According to the existing data, the helminth fauna of true lemmings consists of three widespread and/or locally common taxa: Hymenolepis horrida (sensu lato) (Hymenolepididae), Anoplocephaloides lemmi (Anoplocephalidae) and Heligmosomoides spp. (Heligmosomidae). Despite the taxonomic boundaries and ancient phylogenetic splits in the hosts, there are no major faunistic differences for parasites within western (Siberian) L. sibiricus and L. bungei, and eastern (North American) L. trimucronatus throughout their distribution range. In contrast, the Norwegian lemming L. lemmus, which is a Fennoscandian endemic and closely related to the western populations of L. sibiricus, has only a single host-specific helminth, the cestode Paranoplocephala fellmani n. sp. (Anoplocephalidae). We describe the new species and show that it differs consistently from related species by its long and slender cirrus-sac. However, there are also a number of other significant differences, e.g., P. fellmani n. sp. and Andrya primordialis in Tamiasciurus hudsonicus (Sciuridae) evidently have a unique (sub)type of uterine development among Andrya/Paranoplocephala spp. Because P. fellmani n. sp. was also found to occur in Alaska (host L. trimucronatus), this species seems to follow the same biogeographical pattern as the other specialist helminths of Lemmus. We suggest alternative explanations for the absence of three major helminth taxa in the Norwegian lemming in Fennoscandia.     

Paranoplocephala aquatica n. sp. (Cestoda, Anoplocephalidae) from Arvicola terrestris and Ondatra zibethica (Rodentia), with redescriptions and comments on related species

Paranoplocephala aquatica n. sp. is described from Arvicola terrestris and Ondatra zibethica (Rodentia, Cricetidae) in Bulgaria. The new species is characterised by a band-like strobila, a uterus forming a fine reticulate structure in the early stages of development, numerous testes (approximately 92) situated mainly aporally to the ovary in both the median and the aporal lateral fields, few testes positioned anterior to the ovary and genital ducts, the prominent asymmetrical situation of the female organs, the length of the vagina c. 0.65–0.68 of the length of the cirrus-sac, and the external seminal vesicle covered by a cellular sleeve. The new species is distinguished from P. ondatrae, P. macrocephala, P. dasymidis and P. sciuri. The specimens from O. zibethica reported as P. ondatrae by Tenora & Murai (1980) and as Aprostatandrya macrocephala by Spasskii et al. (1951) are believed to belong to P. aquatica. The type-series of P. ondatrae and P. macrocephala are redescribed and figured; metric data and an illustration of the holotype of P. sciuri are presented. The genus Paranoplocephala sensu Tenora et al. (1986) is regarded as a heterogeneous group because of the two patterns of uterine development in the species studied. Taxonomic criteria used for distinguishing the genera Andrya and Paranoplocephala, and some criteria applicable at the species level, are discussed.     

Morphological and molecular characterisation of Paranoplocephala buryatiensis n. sp. and P. longivaginata Chechulin & Gulyaev, 1998 (Cestoda: Anoplocephalidae) in voles of the genus Clethrionomys

A new species, Paranoplocephala buryatiensis n. sp. (Cestoda:Anoplocephalidae), is described from the grey-sided vole Clethrionomys rufocanus (Sundevall) in the Republic of Buryatia (Russian Federation) and compared with P. longivaginata Chechulin & Gulyaev, 1998, a parasite of the red vole C. rutilus (Pallas) in the same region. P. buryatiensis n. sp. and P. longivaginata both have an exceptionally long vagina and cirrus, unique features among known species of Paranoplocephala Lühe, 1910. The new species differs from P. longivaginata primarily by its wider and more robust body, lower length/width ratio of mature proglottides, tendency of testes to occur in two separate groups, seminal receptacle of a different shape and the position of the cirrus-sac with respect to the ventral longitudinal osmoregulatory canal. The cytochrome oxidase subunit I (COI) sequence data support the independent status of these species, and show that they form a monophyletic assemblage within Paranoplocephala (sensu lato). Assuming cospeciation, an indirect calibration using host speciation dates estimated a rate of mtDNA substitution of 1.0–1.7% pairwise (0.5–0.85% per lineage) sequence divergence per million years. A faunistic review of Paranoplocephala species in C. rufocanus and C. rutilus in the Holarctic region is presented.     

Molecular phylogeny of the speciose vole genus Microtus (Arvicolinae, Rodentia) inferred from mitochondrial DNA sequences

Voles of the genus Microtus represent one of the most speciose mammalian genera in the Holarctic. We established a molecular phylogeny for Microtus to resolve contentious issues of systematic relationships and evolutionary history in this genus. A total of 81 specimens representing ten Microtus species endemic to Europe as well as eight Eurasian, six Asian and one Holarctic species were sequenced for the entire cytochrome b gene (1140 bp). A further 25 sequences were retrieved from GenBank, providing data on an additional 23, mainly Nearctic, Microtus species. Phylogenetic analysis of these 48 species generated four well-supported monophyletic lineages. The genus Chionomys, snow voles, formed a distinct and well-supported lineage separate from the genus Microtus. The subgenus Microtus formed the strongest supported lineage with two sublineages displaying a close relationship between the arvalis species group (common voles) and the socialis species group (social voles). Monophyly of the Palearctic pitymyid voles, subgenus Terricola, was supported, and this subgenus was also subdivided into two monophyletic species groups. Together, these groupings clarify long-standing taxonomic uncertainties in Microtus. In addition, the "Asian" and the Nearctic lineages reported previously were identified although the latter group was not supported. However, relationships among the main Microtus branches were not resolved, suggesting a rapid and potentially simultaneous radiation of a widespread ancestor early in the history of the genus. This and subsequent radiations discernible in the cytochrome b phylogeny, show the considerable potential of Microtus for analysis of historical and ecological determinants of speciation in small mammals. It is evident that speciation is an ongoing process in the genus and that the molecular data provides a vital insight into current species limits as well as cladogenic events of the past.     

Occurrence of a Syngamus sp. in tundra voles (Microtus oeconomus) collected on St. Lawrence Island, Bering Sea.

A species of syngamid nematode belonging to the genus Syngamus was found in the respiratory tract (terminal trachea to bronchi) of tundra voles (Microtus oeconomus) collected on St. Lawrence Island, Alaska (USA). Its prevalence in June 1989 was greater than 29% (12 of 41 male voles and seven of 24 females) in the village of Savoonga, while no nematodes were found from 41 voles collected in the village of Gambell. Lesions included dilatation of parasitized respiratory ducts and peribronchial and perivascular cuffing by lymphoid cells, mainly plasma cells, in parasitized lobes. Morphologically, this syngamid species differed from S. microtinae reported previously from the same host species as well as from other syngamids known from avian hosts.     

Cytosolic isocitrate dehydrogenase in humans, mice, and voles and phylogenetic analysis of the enzyme family

In this study, we report cDNA sequences of the cytosolic NADP-dependent isocitrate dehydrogenase for humans, mice, and two species of voles (Microtus mexicanus and Microtus ochrogaster). Inferred amino acid sequences from these taxa display a high level of amino acid sequence conservation, comparable to that of myosin beta heavy chain, and share known structural features. A Caenorhabditis elegans enzyme that was previously identified as a protein similar to isocitrate dehydrogenase is most likely the NADP-dependent cytosolic isocitrate dehydrogenase enzyme equivalent, based on amino acid similarity to mammalian enzymes and phylogenetic analysis. We also suggest that NADP-dependent isocitrate dehydrogenases characterized from alfalfa, soybean, and eucalyptus are most likely cytosolic enzymes. The phylogenetic tree of various isocitrate dehydrogenases from eukaryotic sources revealed that independent gene duplications may have given rise to the cytosolic and mitochondrial forms of NADP-dependent isocitrate dehydrogenase in animals and fungi. There appears to be no statistical support for a hypothesis that the mitochondrial and cytosolic forms of the enzyme are orthologous in these groups. A possible scenario of the evolution of NADP-dependent isocitrate dehydrogenases is proposed.      

Co-occurrence of ectoparasites on rodent hosts: null model analyses of data from three continents

We studied patterns of species co-occurrence in communities of ectoparasitic arthropods (ixodid ticks, mesostigmate mites and fleas) harboured by rodent hosts from South Africa ( Rhabdomys pumilio ), South America ( Scapteromys aquaticus and Oxymycterus rufus ) and west Siberia ( Apodemus agrarius , Microtus gregalis , Microtus oeconomus and Myodes rutilus ) using null models. We compared frequencies of co-occurrences of parasite species or higher taxa across host individuals with those expected by chance. When non-randomness of parasite co-occurrences was detected, positive but not negative co-occurrences of parasite species or higher taxa prevailed (except for a single sample of mesostigmate mites from O. rufus ). Frequency of detection of non-randomness of parasite co-occurrences differed among parasite taxa, being higher in fleas and lower in mites and ticks. This frequency differed also among host species independent of parasite taxon, being highest in Microtus species and lowest in O. rufus and S. aquaticus . We concluded that the pattern of species co-occurrence in ectoparasite communities on rodent hosts is predominantly positive, depends on life history of parasites and may be affected to a great extent by life history of a host.     

Sex chromosomes pairing in two Arvicolidae species: Microtus nivalis and Arvicola sapidus

Arvicolid rodents present both synaptic and asynaptic sex chromosomes. We analyzed the pairing behaviour of sex chromosomes in two species belonging to this rodent group (Microtus nivalis and Arvicola sapidus). At pachynema, the sex chromosomes of both species paired in a small region while the rest remain unsynapsed. Consequently at metaphase I, sex chromosomes present end-to-end association. Thus, the pairing behaviour of sex chromosomes in these species is very similar to that previously described for other arvicolid rodents and for most mammals. According to this, we propose that synaptic sex chromosomes were the ancestral condition in the family Arvicolidae, including the genus Microtus. The phylogenetic origin of the asynaptic sex chromosomes in the genus Microtus would have arisen once in the lineage that originated the species M. arvalis/agrestis and related species, while the lineage that originated the species M. oeconomous and related species conserved synaptic chromosomes. Furthermore, the phylogenetic relationships between the genus Microtus, Chionomys and Pitymys are discussed in relation to the synaptic behaviour of sex chromosomes.     

First report of Siphonaptera infesting Microtus (Microtus) cabrerae (Rodentia-Muridae-Arvicolinae) in Cuenca,Spain and notes about the morphologic variability of Ctenophthalmus (Ctenophthalmus) apertus personatus (Insecta-Siphonaptera-Ctenophthalmidae)

The fleas infesting Microtus (Microtus) cabrerae from three different areas of Cuenca province (Spain) have been studied. It is the first time that on ectoparasitological study of this badly known rodent has been done. Four Siphonaptera species have been detected: Rhadinopsylla (Actenophthalmus) pentacantha, Peromyscopsylla spectabilis spectabilis, Nosopsyllus fasciatus and Ctenophthalmus (Ctenophthalmus) apertus personatus, which was the most abundant species (26 males and 31 females of a total of 28 males and 35 females). Considering the great morphologic variability within the male processus basimerus ventralis (p.b.v.) of segment IX of C. personatus subspecies, three morphotypes have been recognised. The male polymorphism detected, would be the result of both host confinement and genetic selection acting on the parasite. It should be pointed out that C. (C.) apertus personatus is not narrowly host-specific, therefore further studies are required to clarify this taxonomic situation.     

Size of the vomeronasal organ in wild Microtus with different mating strategies

Most studies on mammalian vomeronasal organ (VNO) have been on laboratory-bred animals. Our present study examines the VNO in wild-caught meadow voles (Microtus pennsylvanicus: n=16) and prairie voles (M. ochrogaster: n=15). These species vary in their mating strategies and degree of parental care by males. M. ochrogaster exhibits pair bonding and more paternal care compared to M. pennsylvanicus, a promiscuous species. We hypothesize that sexual dimorphism will occur in the promiscuous species based on previous studies which suggest that those who exhibit more aggressive or masculine behavior have larger VNOs. Our results support our original finding that VNOs are not different in size in wild Microtus spp. that vary in male parental tendencies. However, the present study also indicates that M. pennsylvanicus, the species exhibiting more disparate parental tendencies, exhibited larger VNOs in females than males. This is the reverse of previous findings on rats, and we hypothesize that this difference may be due to mate selectivity and/or maternal aggression.     

Effects of vaginal-cervical stimulation in seven species of muroid rodents.

Six species of muroid rodents (Peromyscus californicus, P. eremicus, P. gossypinus, Mesocricetus auratus, Rattus norvegicus and R. rattus) were given artificlal vaginal-cervical stimulation in an attempt to induce pseudopregnancy. Some females of each species became pseudopregnant, but it was not clear that stimulation patterns mimicking the copulatory patterns of conspecific males were more effective than other patterns of stimulation. In the non-domesticated species (Peromyscus and R. rattus) a few females responded to a variety of stimulus conditions, and no species differences in responsiveness among the wild species were evident. The established laboratory rodents (R. norvegicus, M. auratusy were markedly more responsive to artificial stimulation, suggesting possible effects of domestication on fecundity and reactions to handling- Microtus ochrogaster, an induced ovulator, ovulated in response to vaginal-cervical stimulation only if one intromission from a male was also provided. No other differences in the responses of reflex and spontaneous ovulators were apparent.     

Mitochondrial cytochrome b sequence yields new insight into the speciation of social voles in south-west Asia

We established a cytochrome b (cyt b ) phylogeny for six species of social voles. A Bayesian approach to phylogenetic reconstruction (BI) and a maximum likelihood (ML) tree revealed a dichotomy into two major clusters, namely a Microtus guentheri cluster and a M. socialis cluster. The three main lineages that emerged within each of these two clusters were separated by the K2P divergences which are above the intraspecific variation in Microtus . All six species were also retrieved in the minimum spanning network. Within its present taxonomic scope, M. guentheri is paraphyletic and consists of two allopatric sibling species: M. guentheri (Syria, Israel) and M. hartingi (Anatolia and the Balkans). The closest relative to these two species is M. dogramacii , which is possibly a sister species to M. hartingi . The two geographic samples were identified as M. irani , one from Shiraz (Iran) and the other from Balkusan (Turkey). The cyt b sequence confirmed the specific status of M. anatolicus within the M. socialis cluster. Although five species of social voles occur within a radius of < 500 km in the north-eastern corner of the Mediterranean, small-scale sympatry is exceptional. Species richness in this region possibly originates from past fragmentation with subsequent allopatric speciation in refugial areas.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 121–128.