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.     

Glacial survival of the Norwegian lemming (Lemmus lemmus) in Scandinavia: inference from mitochondrial DNA variation

In order to evaluate the biogeographical hypothesis that the Norwegian lemming (Lemmus lemmus) survived the last glacial period in some Scandinavian refugia, we examined variation in the nucleotide sequence of the mitochondrial control region (402 base pairs (bp)) and the cytochrome b (cyt b) region (633 bp) in Norwegian and Siberian (Lemmus sibiricus) lemmings. The phylogenetic distinction and cyt b divergence estimate of 1.8% between the Norwegian and Siberian lemmings suggest that their separation pre-dated the last glaciation and imply that the Norwegian lemming is probably a relic of the Pleistocene populations from Western Europe. The star-like control region phylogeny and low mitochondrial DNA diversity in the Norwegian lemming indicate a reduction in its historical effective size followed by population expansion. The average estimate of post-bottleneck time (19-21 kyr) is close to the last glacial maximum (18-22 kyr BP). Taking these findings and the fossil records into consideration, it seems likely that, after colonization of Scandinavia in the Late Pleistocene, the Norwegian lemming suffered a reduction in its population effective size and survived the last glacial maximum in some local Scandinavian refugia, as suggested by early biogeographical work.     

Metabolic rate and thermal conductance of lemmings from high-arctic Canada and Siberia

The arctic climate places high demands on the energy metabolism of its inhabitants. We measured resting (RMR) and basal metabolic rates (BMR), body temperatures, and dry and wet thermal conductances in summer morphs of the lemmings Dicrostonyx groenlandicus and Lemmus trimucronatus in arctic Canada, and the BMR of D. torquatus, D. groenlandicus, L. sibiricus, L. bungei and L. trimucronatus in Siberia. In contrast to previous studies the data were collected on animals that had spent only a limited time in captivity. All parameters were analysed in relation to the variations in body mass (20-90 g). Body temperature and BMR were lower in D. groenlandicus than L. trimucronatus, which coincides with greater longevity in the former species. Wet and dry thermal conductances of both species were similar and comparable with those of other Myomorpha (mouse-type rodents), indicating no evidence for a previously claimed lower thermal conductance in lemmings. BMR in lemmings appeared to be higher than in other Arvicolidae (voles, lemmings and muskrats), which could relate to their typically high-latitude distribution. However, the more southerly living Lemmus species had higher BMR than the more northerly living Dicrostonyx species, which may be explained by the former having a relatively low-quality diet.     

Morphotypic variability of masticatory surface pattern of molars in the recent and Pleistocene Lemmus and Myopus (Rodentia,Cricetidae) of Europe and Western Siberia

In this article, we present the results of morphological study, applying multivariate statistical analysis, of seven samples of recent Lemmini species (Lemmus lemmus, L. sibiricus, Myopus schisricolor) and eight samples of the ancient Siberian lemmings from the Middle and Late Pleistocene localities, mainly in northeastern Europe. On the basis of studying variability of masticatory surface pattern of molars, 24 morphotypes have been described. The differences in morphotypes frequencies were found between the recent Myopus and Lemmus and between the two Norwegian lemming samples. There are some indications of an evolutionary trend in molar morphology of the Siberian lemmings of the Middle, Late Pleistocene, and the recent of Eastern Europe. The distinctions, at least, between the Middle Pleistocene and modern lemmings exceed a species level.     

Genetic and morphometric variation in the Holarctic helminth parasite Andrya arctica (Cestoda, Anoplocephalidae) in relation to the divergence of its lemming hosts (Dicrostonyx spp.)

Andrya arctica is a cestode parasite of the family Anoplocephalidae (Cyclophyllidea), parasitizing lemmings of the genus Dicrostonyx throughout the Holarctic region. The population structure of this intestinal parasite was studied from eight different regions, six of which represented different genetic entities of lemming hosts. Molecular sequence tagged site markers and minisatellite fingerprints as well as morphology and morphometries were used to reveal the population structure of A. arctica in the Holarctic region. The results suggest that the evolutionary history of this cestode species has included different processes acting on different geographical regions. On the Siberian mainland (host D. torquatus), the division of the parasites into different genetic entities agreed perfectly with the chromosomal races of the lemming hosts that points towards a shared evolutionary history between the host and the parasite ('cospeciation'). The main phylogenetic split of Dicrostonyx between Eurasia and North America was not, however, observed in A. arctica. This suggests that in the Nearctic (host D. groenlandicus) the parasite has remained relatively unmodified because of the large cohesive populations ('coadaptation'). The uniqueness of the Greenland population, and possibly also that of the Wrangel Island, can be explained by peripheral isolation, refugial effects or founder effects.     

Shedding new light on the diet of Norwegian lemmings: DNA metabarcoding of stomach content

Lemmings are key herbivores in many arctic food webs, and their population dynamics have major impacts on the functioning of tundra systems. However, current knowledge of lemming diet is limited, hampering evaluation of lemming–vegetation interactions. This lack of knowledge is mainly due to methodological challenges, as previously used microhistological methods result in large proportions of poorly resolved plant taxa. We analyzed diets of Norwegian lemmings (Lemmus lemmus) in three different habitats using a new method, DNA metabarcoding of stomach contents. To achieve detailed information on ingested vascular plants, bryophytes, and fungi, we amplified short fragments of chloroplast DNA (for plants; P6 loop of the trnL intron) and nuclear ribosomal DNA (for fungi; ITS1-region). Our results revealed that lemming diets were dominated by grasses, mainly Avenella flexuosa, and mosses, mainly Dicranum spp., but that a variety of other food items were also eaten. Vascular plant composition of the diets differed between heath, meadow, and wetland habitats, whereas bryophyte composition did not. Also, a variety of fungal taxa were retrieved, but as most of the identified taxa belong to micromycetes, they were unlikely to be consumed as food. The role of fungi in the diet of lemmings remains to be investigated. We suggest that there may be substantial variation between habitats and regions in lemming diet.     

The topography of Gomori positive neurosecretory elements of the hypothalamus of the lemmings Dicrostonyx torquatus and Lemmus sibiricus]

Under study was the structure of the hypothalamo-hypophyseal neurosecretory system in two species of lemmings of the Wrangel island: the collared lemming, (Dicrostonyx torquatus) and the Ob lemming (Lemmus sibiricus). Inspite of the similarity in the general organization of this system in all rodents, certain species features were found in the topography of neurosecretory elements in the animals studied. In the Ob lemming there is a great similarity in the structures of the neurosecretory system with the albino rat than in the collared lemming. In both species of lemmings, and in the collared lemming in particular, the supraoptic nucleus is located more dorso-caudally and the paraventricular one-more dorsally. A greater amount of neurosecretory cells is found which from additional groups. The hypothalamo-hypophyseal and extrahypothalamic pathways are well pronounced. The postoptical nucleus is considerably developed. In the collared lemming it is almost equal to the supraoptic one in the amount of cells composing it. The ratio of the cells in the supraoptic and postoptic nuclei is suggested to be related to the level of the water-salt metabolism and the specific ecology of lemmings.     

Comparing the genetic population structure of two species of arctic lemmings: more local differentiation in Lemmus trimucronatus than in Dicrostonyx groenlandicus

Collared and brown lemmings ( Dicrostonyx groenlandicus and Lemmus trimucronatus ) are two largely sympatric and ecologically comparable species of arctic microtine rodents, differing however in some respects which allow us to hypothesise differences in the genetic structure of their populations. Collared lemmings are particularly well adapted to life at high latitude, they occasionally emerge to the surface of the snow and may disperse over larger distances than brown lemmings – possibly even over snow and ice. This should result in more local differentiation among populations of brown lemmings than among populations of collared lemmings. We compared the genetic population structure between the two lemming species in a fragmented landscape with small islands in the central Canadian Arctic using four microsatellite loci and partial mitochondrial control region sequences. Both types of genetic markers showed higher differentiation ( F _ST values) among local populations for brown lemmings than for collared lemmings. We discuss to what extent the observed genetic differences may be explained by differences in dispersal rates in addition to differences in average effective population size.     

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.     

Predator–prey relationships: arctic foxes and lemmings

1. The number of breeding dens and litter sizes of arctic foxes Alopex lagopus were recorded and the diet of the foxes was analysed during a ship-based expedition to 17 sites along the Siberian north coast. At the same time the cyclic dynamics of co-existing lemming species were examined.
2. The diet of arctic foxes was dominated by the Siberian lemming Lemmus sibiricus (on one site the Norwegian lemming L. lemmus ), followed by the collared lemming Dicrostonyx torquatus .
3. The examined Lemmus sibiricus populations were in different phases of the lemming cycle as determined by age profiles and population densities.
4. The numerical response of arctic foxes to varying densities of Lemmus had a time lag of 1 year, producing a pattern of limit cycles in lemming–arctic fox interactions. Arctic fox litter sizes showed no time lag, but a linear relation to Lemmus densities. We found no evidence for a numerical response to population density changes in Dicrostonyx .
5. The functional or dietary response of arctic foxes followed a type II curve for Lemmus , but a type III response curve for Dicrostonyx .
6. Arctic foxes act as resident specialist for Lemmus and may increase the amplitude and period of their population cycles. For Dicrostonyx , on the other hand, arctic foxes act as generalists which suggests a capacity to dampen oscillations.     

Ecology of the Siberian Lemming (Lemmus sibiricus) and the Distribution History of the Collared Lemming (Dicrostonyx torquatus) (Rodentia,Cricetidae) on the New Siberian Islands

Biology Bulletin - One hundred twenty Siberian lemmings (Lemmus sibiricus) were studied from Kotelnyi Island in the eastern sector of the Polar basin. The main habitats, abundance, nutrition,...     

New distribution records of Echinococcus multilocularis in the brown lemming from Barrow, Alaska, USA

We identified Echinococcus multilocularis for the first time in brown lemmings (Lemmus trimucronatus) from Barrow, Alaska, USA. Of 467 brown lemmings trapped between 1995 and 2000, two males and two females (0.9%; 95% confidence interval=0.9+/-0.9%) were found to be infected with metacestodes of E. multilocularis. No metacestodes were found in 17 collared lemmings (Dicrostonyx rubricatus) also trapped at Barrow. In humans, E. multilocularis causes alveolar echinococcosis, which is potentially fatal. Knowledge of the distribution of this parasite is important to protect the public health.     

Description of Paranoplocephala etholeni n. sp. (Cestoda: Anoplocephalidae) in the meadow vole Microtus pennsylvanicus,with a synopsis of Paranoplocephala s. l. in holarctic rodents

Paranoplocephala etholeni n. sp., parasitizing the meadow vole Microtus pennsylvanicus in Alaska and Wisconsin, USA, is described. Paranoplocephala etholeni is morphologically most closely related to the Nearctic Paranoplocephala ondatrae (Rausch, 1948). Available data suggest that P. etholeni is a host-specific, locally rare species that may have a wide but sporadic geographical distribution in North America. The finding of P. ondatrae-like cestodes in Microtus spp. suggests that this poorly known species may actually be a parasite of voles rather than muskrat (type host). A tabular synopsis of all the known species of Paranoplocephala s. l. in the Holarctic region with their main morphological features is presented.     

Benefiting from a migratory prey: spatio-temporal patterns in allochthonous subsidization of an Arctic predator

1.?Flows of nutrients and energy across ecosystem boundaries have the potential to subsidize consumer populations and modify the dynamics of food webs, but how spatio-temporal variations in autochthonous and allochthonous resources affect consumers' subsidization remains largely unexplored. 2.?We studied spatio-temporal patterns in the allochthonous subsidization of a predator living in a relatively simple ecosystem. We worked on Bylot Island (Nunavut, Canada), where arctic foxes (Vulpes lagopus L.) feed preferentially on lemmings (Lemmus trimucronatus and Dicrostonyx groenlandicus Traill), and alternatively on colonial greater snow geese (Anser caerulescens atlanticus L.). Geese migrate annually from their wintering grounds (where they feed on farmlands and marshes) to the Canadian Arctic, thus generating a strong flow of nutrients and energy across ecosystem boundaries. 3.?We examined the influence of spatial variations in availability of geese on the diet of fox cubs (2003-2005) and on fox reproductive output (1996-2005) during different phases of the lemming cycle. 4.?Using stable isotope analysis and a simple statistical routine developed to analyse the outputs of a multisource mixing model (SIAR), we showed that the contribution of geese to the diet of arctic fox cubs decreased with distance from the goose colony. 5.?The probability that a den was used for reproduction by foxes decreased with distance from the subsidized goose colony and increased with lemming abundance. When lemmings were highly abundant, the effect of distance from the colony disappeared. The goose colony thus generated a spatial patterning of reproduction probability of foxes, while the lemming cycle generated a strong temporal variation of reproduction probability of foxes. 6.?This study shows how the input of energy owing to the large-scale migration of prey affects the functional and reproductive responses of an opportunistic consumer, and how this input is spatially and temporally modulated through the foraging behaviour of the consumer. Thus, perspectives of both landscape and foraging ecology are needed to fully resolve the effects of subsidies on animal demographic processes and population dynamics.     

Checklist of helminth parasites of the cane toad Bufo marinus (Anura: Bufonidae) from Mexico

Thirty-four adult cane toads Bufo marinus L. (12 males and 22 females) collected from 2 localities in Mexico (Cerro de Oro and Temascal Dams, Oaxaca) in September 2003 were examined for helminth parasites. In total, 14,749 helminths belonging to 14 taxa were collected. Included were 2 adult digeneans (Choledocystus hepaticus, Mesocoelium monas); 1 larval cestode (an unidentified pseudophyllidean); and 11 nematodes, including 3 species of larvae (Contracaecum sp., Physaloptera sp., Physocephalus sexalatus) and 8 species of adults (Aplectana itzocanensis, Cosmocerca sp., Cruzia morleyi, Ochoterenella digiticauda, Oswaldocruzia sp., Raillietnema sp., Rhabdias americanus, and Rhabdiasfuelleborni). Higher species richness was recorded in B. marinus from Cerro de Oro (12 taxa versus 9 in those from Temascal); hosts from both localities shared 7 taxa. There were 25 new locality records, and 2 taxa were registered in Mexico for the first time. To date, 112 helminth species have been recorded parasitizing B. marinus along its native and introduced range of distribution, with 40.5% of them reported from Mexico.     

Isolation and Characterization of a Hantavirus from Lemmus sibiricus: Evidence for Host Switch during Hantavirus Evolution

A novel hantavirus, first detected in Siberian lemmings (Lemmus sibiricus) collected near the Topografov River in the Taymyr Peninsula, Siberia (A. Plyusnin et al., Lancet 347:1835-1836, 1996), was isolated in Vero E6 cells and in laboratory-bred Norwegian lemmings (Lemmus lemmus). The virus, named Topografov virus (TOP), was most closely related to Khabarovsk virus (KBR) and Puumala viruses (PUU). In a cross focus reduction neutralization test, anti-TOP Lemmus antisera showed titers at least fourfold higher with TOP than with other hantaviruses; however, a rabbit anti-KBR antiserum neutralized TOP and KBR at the same titer. The TOP M segment showed 77% nucleotide and 88% amino acid identity with KBR and 76% nucleotide and 82% amino acid identity with PUU. However, the homology between TOP and the KBR S segment was disproportionately higher: 88% at the nucleotide level and 96% at the amino acid level. The 3' noncoding regions of KBR and the TOP S and M segments were alignable except for 113- and 58-nucleotide deletions in KBR. The phylogenetic relationships of TOP, KBR, and PUU and their respective rodent carriers suggest that an exceptional host switch took place during the evolution of these viruses; while TOP and KBR are monophyletic, the respective rodent host species are only distantly related.     

Development of the acrosomic system of the spermatozoon in the Norwegian lemming (Lemmus lemmus)

Summary An electronmicroscopic study on the development of the acrosome system of the spermatozoon in the Norwegian lemming (Lemmus lemmus) has been performed. The proacrosomal granules were found to be few and to consist of a dense center and a less dense periphery, and the acrosomal vesicle to contain stainable material of the same structure but of lower density than that of the acrosomal granule. Like in the guinea pig, two zones of different density exist throughout acrosome development and are visible also in mature spermatozoa. A large osmiophilic formation consisting of saccular, tubular, and lamellar structures, was found between the apex of the condensed nucleus and the acrosome and was identified as perforatorium.We are greatly thankful to Dr. Antti Telkkä, and Mr. Mauri Nyholm, M. Sc. for expert advise in electronmicroscopy and Mr. P. Lehtimäki for photographic help. For the supply of the lemmings we are indebted to Prof. K. Lagerspetz, and Mr. O. Hissa, M. Sc. This work is related to a series of studies on the biology of the Norwegian lemming (for previous works see Asp et al.).