Does the morphology of the ear of the Chinese bamboo rat (Rhizomys sinensis) show “Subterranean” characteristics?

In spite of the growing interest in rodents with subterranean activity in general and the spalacids (Spalacidae) in particular, little is known about the biology of most members of this clade, such as the Chinese bamboo rat (Rhizomys sinensis). Here, we analyzed the ear morphology of R. sinensis with respect to hearing specialization for subterranean or aboveground modes of communication. It is well‐known that ecology and style of life of a particular species can be reflected in morphology of its ear, its hearing and vocalization, so we expect that such information could provide us insight into its style of life and its sensory environment. The ratio between the eardrum and stapedial footplate areas, which influences the efficiency of middle ear sound transmission, suggests low hearing sensitivity, as is typical for subterranean species. The cochlea had 3.25 coils and resembled species with good low frequency hearing typical for subterranean mammals. The length of the basilar membrane was 18.9 ± 0.8 mm and its width slowly increased towards the cochlear apex from 60 to 85 μm. The mean density of outer hair cells was 344 ± 22 and of inner hair cells 114 ± 7.3 per 1 mm length of the organ of Corti, and increased apically. These values (except for relatively low hair cell density) usually characterize ears specialized for low frequency hearing. There was no evidence for an acoustic fovea. Apart of low hair cell density which is common in aboveground animals, this species has also relatively large auricles, suggesting the importance of sound localization during surface activity. The ear of the Chinese bamboo rat thus contains features typical for both aboveground and subterranean mammals and suggests that this spalacid has fossorial habits combined with regular aboveground activity. J. Morphol. 277:575–584, 2016. © 2016 Wiley Periodicals, Inc.     

Detection of the larva of Taenia multilocularis in 2 voles (Microtus arvalis and Clethrionomys glareolus) in a focus of alveolar echinococcosis in the Massif Central (France)

Small wild rodents were collected and examined during 1983-1984 to investigate parasite-host relationships of Echinococcus multilocularis in one habitat suitable for red foxes of Auvergne (France). The natural infestation of the liver of two different voles, Microtus arvalis and Clethrionomys glareolus, by the larval stage of the cestode is recorded for the first time. In the both cases, the larvae were fully developed and numerous protoscolices were present with some calcareous corpuscules; the expansion of the larvae involved several hepatic lobes in Microtus and was restricted to a single lobe in Clethrionomys. Epidemiological consequences of the receptivity of the two hosts are not yet investigated in the field. However several species of voles inhabiting the same endemic area and which are receptive to the larval stage of alveolar echinococcosis should be a favourable factor of durability for the cestodiasis of the foxes; so the parasite is able of surviving the cyclic and considerable but not simultaneous fluctuations of the three populations of voles which are locally implicated in the zoonosis: M. arvalis, C. glareolus and Arvicola terrestris, by changing from one species to the others.     

甘肃鼢鼠和根田鼠听域研究

用电生理学方法对甘肃鼢鼠和根田鼠的听性脑干反应(ABR)的反应阈值做了测定,以确定甘肃鼢鼠和根田鼠听域.结果 表明甘肃鼢鼠听力敏感频率为12 kHz,根田鼠的听力敏感频率为16～32 kHz.甘肃鼢鼠和根田鼠听性脑干电位测定结果表明地下鼠和地面鼠低频高频听力阈值存在差异,地下鼠对中低频声波敏感.     

Acoustic communication and burrow acoustics are reflected in the ear morphology of the coruro (Spalacopus cyanus, Octodontidae), a social fossorial rodent

We studied the middle and inner ears of seven adult coruros (Spalacopus cyanus), subterranean and social rodents from central Chile, using free-hand dissection and routine staining techniques. Middle ear parameters that were focused on here (enlarged bullae and eardrums, ossicles of the "freely mobile type") are believed to enhance hearing sensitivity at lower frequencies. The organ of Corti was of a common mammalian type and revealed three peaks of higher inner hair cell densities. Based on a position frequency map, frequencies were assigned to the respective peaks along the basilar membrane. The first peak at around 300-400 Hz is discussed with respect to the burrow acoustics, while the peak around 10-20 kHz is probably a plesiomorphic feature. The most pronounced peak at around 2 kHz reflects the frequency at which the main energy of vocal communication occurs. The morphology of the ear of the coruro corresponds to the typical pattern seen in subterranean rodents (low frequency and low-sensitivity hearers), yet, at the same time, it also deviates from it in several functionally relevant features.     

Expression patterns of clock genes in the hypothalamus and eye of two Lasiopodomys species

ABSTRACT

To investigate the relationship between light sensing systems in the eye and circadian oscillators in the hypothalamus of subterranean rodents, we studied subterranean Mandarin voles (Lasiopodomys mandarinus) that spend their entire lives under dark conditions with degenerated eyes, and compared oscillatory expression patterns of clock genes in the hypothalamus and eye between Mandarin voles and their aboveground relatives, Brandt’s voles (L. brandtii). Individuals of both vole species were kept under a 12-h light/12-h dark condition or continuous dark condition for 4 weeks. In both species, the expressions of most genes showed significant cosine rhythmicity in the hypothalamus but relatively weak rhythmicity in the eye. The number of rhythmic genes in the eye of Mandarin voles increased under the dark condition, but the opposite trend was observed in the eye of Brandt’s voles. The expression levels of most clock genes in the hypothalamus of both vole species did not significantly differ between the two conditions, but unlike in Mandarin voles, these expression levels significantly decreased in the eye of Brandt’s voles kept under the dark condition. In both vole species, the peak phase of most clock genes exhibited advanced or invariant change in the hypothalamus under the dark condition, and the peak phase of most clock genes showed consistent changes between the eye and hypothalamus of Mandarin voles. However, most clock genes in the eye showed a delayed phase in Brandt’s voles kept under the dark condition. In conclusion, the hypothalamus plays an important role in both vole species irrespective of the light condition. However, the expression patterns of clock genes in the eye differed between the vole species, indicating that each species adapted differently to their environments.     

Gamasid mites of common voles in the central Volga River region

The specific composition of gamasid mites from three species of voles (Microtus arvalis Pall., M. agrestis L., M. oeconomus Pall.) is given. Forest, field and flood-land groupings of the common vole having distinct phenotypical differences are characterized by differences in the structure of their parasite fauna. In the forest the number of meadow and meadow-field species decreases while that of forest species of mites regularly increases.     

Possible atypical course of tularemia (persistence) in the common vole Microtus arvalis Pall

The possibility of the atypical course of tularemia with the prolonged persistence of Francisella tularensis in common voles (M. arvalis), the twin species of East European voles (M. rossiaemeridionalis), was studied. Experiments were made on 33 animals grown in the laboratory. F. tularensis strain 165 was used. The animals were infected by feeding them according to the previously developed scheme. 7 out of 33 voles showed the atypical course of tularemia: in 3 voles the disease took a prolonged course with bacteriuria and death on days 25-34; 3 other voles with bacteriuria registered before days 33, 66 and 172 (the term of observation) survived. The surviving animals were killed on day 183, and the presence of bacteria in their organs and seroconversion were established. One vole excreted no bacteria with urine and had no bacteria in its organs (the animal was examined on day 156), but in its blood specific antibodies were detected. To determine bacteriuria, the immunofluorescence test was used together with biological assays. Thus, M. arvalis, like M. rossiaemeridionalis studied earlier, can harbor F. tularensis at the period between epizootics. When voles of the former species penetrate stacks of straw and hayricks, conditions appear for the transfer of the infection to the latter species, M. rossiaemeridionalis. Therefore, in the foci of the meadow-field type each of these two species of voles may be not only of epizootic, but also of epidemic importance.     

Holarctic phylogeography of the root vole (Microtus oeconomus): implications for late Quaternary biogeography of high latitudes

A species-wide phylogeographical study of the root vole (Microtus oeconomus) was performed using the whole 1140 base pair mitochondrial (mt) cytochrome b gene. We examined 83 specimens from 52 localities resulting in 65 unique haplotypes. Our results demonstrate that the root vole is divided into four main mtDNA phylogenetic lineages that seem to have largely allopatric distributions. Net divergence estimates (2.0-3.5%) between phylogroups, as well as relatively high nucleotide diversity estimates within phylogroups, indicate that the distinct phylogeographical structure was initiated by historical events that predated the latest glaciation. European root voles are divided into a Northern and a Central mtDNA phylogroup. The mtDNA data in concert with fossil records imply that root voles remained north of the classical refugial areas in southern Europe during the last glacial period. The currently fragmented populations in central Europe belong to a single mtDNA phylogroup. The Central Asian and the North European lineages are separated by the Ural Mountains, a phylogeographical split also found in collared lemmings (Dicrostonyx) and the common vole (M. arvalis). The Beringian lineage occurs from eastern Russia through Alaska to northwestern Canada. This distribution is congruent with the traditional boundaries of the Beringian refugium and with phylogeographical work on other organisms. In conclusion, similarities between the phylogeographical patterns in the root vole and other rodents, such as Arctic and subarctic lemmings, as well as more temperate vole species, indicate that late Quaternary geological and climatic events played a strong role in structuring northern biotic communities.     

A comparative study of isolation-induced ultrasonic vocalization in rodent pups.

The purpose of this study was to determine whether species differences in neonatal vocalizations of rodent pups could be observed. Ultrasonic vocalizations of pups of 5 rodent species, mouse (ICR), vole (Microtus arvalis), Syrian hamster, rat (Wistar-Imamichi), and Mongolian gerbil were recorded from 3 to 15 or 21 days of age. Recordings were made under conditions of separation from mothers and litter mates in a cooled chamber (approximately 10 degrees C). The major species differences observed were age specific and species specific frequencies. The Mongolian gerbil displayed a different frequency change with age. Namely, the day on which ultrasonic vocalizations ceased was delayed in Mongolian gerbil compared with the other rodents. The modal peak frequencies of ultrasound emitted from pups at 3 days of age were low (around 35 kHz) in the vole and the Syrian hamster, medium (around 45 kHz) in the rat and the Mongolian gerbil, and high (around 55 kHz) in the mouse.     

Breeding and rearing of Japanese field voles (Microtus montebelli Milne-Edwards) and Hungarian voles (Microtus arvalis Pallas) as new herbivorous laboratory animal species

Microtus species are very useful as experimental small animals with herbivorous characteristics. In this report, to approach establishment of the use of Japanese field voles (M. montebelli) and Hungarian voles (M. arvalis) as experimental animals, the biological characteristics, breeding methods and reproductive performance of these animal species were comparatively investigated. The number of chromosomes of M. arvalis is 12n = 46, differing from those of M. montebelli, 2n = 30. The breeding and reproduction of the Microtus species were relatively easily accomplished in the laboratory, by giving high fiber-containing rations. These animals prove to be polyestrous and showed postpartum estrous on the day of parturition. In the breeding by the continuous mating of the same pair, there was little or no delay in implantation due to lactation, especially in M. arvalis resulting in continuous birth at intervals of 20 to 21 days. On examination of vaginal smears, Japanese field voles (M. montebelli) did not show any definite pattern whereas 23 out of 30 voles from Hungary (M. arvalis) examined showed 6- to 18-day cycles. There were remarkable differences between the Japanese voles and the Hungarian voles, both biologically and reproductively.     

Frenkelia parasites in a small mammal community. Dynamics of infection and effect on the host

A community of small mammals, Clethrionomys glareolus, Arvicola terrestris, Microtus arvalis, M. agrestis, M. subterraneus, Apodemus spp. and Sorex spp., was studied as hosts of Frenkelia glareoli and F. microti in Fronche-Comté (France). They were monitored in spring, summer and autumn on an area of about 1,350 ha comprising open field, hedgerow network and forest. Among 1,714 small mammals examined between July 1992 and October 1993, 47% (178/376) of C. glareolus, 9.9% (14/139) of A. terrestris and 1.3% (4/311) of Apodemus spp. were infected by F. glareoli. The prevalence of infection with F. microti was 9.2% (66/716) in M. arvalis and 8.2% (6/73) in M. agrestis. M. subterraneus and Sorex spp. were not infected. The maintenance of each parasite in a rural landscape is assured both by a forest and a grassland host. Multiple logistic regression showed that prevalence was highly age-dependent, with an apparent seasonal pattern. Prevalence varied between 30% in summer and 60% in early spring for F. glareoli in C. glareolus and between 3% in autumn to 30% in early spring for F. microti in M. arvalis. The year, habitat, host sex, relative density had no impact on prevalence. In M. arvalis only, sexually active voles were preferentially uninfected, indicating a possible impact of this parasitism on fertility.     

Hearing in coruros (<Emphasis Type="Italic">Spalacopus cyanus</Emphasis>): special audiogram features of a subterranean rodent

Learning curves and behavioural audiograms of subterranean, socially living coruros (Spalacopus cyanus) were obtained using a positive reinforcement conditioning procedure. The individually varying audiograms revealed best hearing at frequencies between 1.25 and 1.6 kHz, which corresponds with the common pattern established in subterranean rodents studied so far. However, the broad hearing range covering frequencies at least between 0.25 and 20 kHz coupled with the high sensitivity (average minimum 7 dB) that is found in coruros are atypical features for audiograms of subterranean rodents, which usually show restricted high-frequency hearing ranges and very poor sensitivity. Hearing at low frequencies (peaks at frequencies <1 kHz), which may be related to sound transmission in underground burrows, and high sensitivity at 1.25/1.6 kHz are discussed in relation to vocalization. In addition to these peaks, a third peak at 8 kHz—probably a plesiomorphic feature of mammals—may be of significance in aboveground communication.     

Phylogeography of the common vole (Microtus arvalis) with particular emphasis on the colonization of the Orkney archipelago

To investigate the human introduction of the common vole Microtus arvalis onto the Orkney islands, the complete cytochrome b gene was sequenced in 41 specimens from both Orkney (four localities) and elsewhere in their range (26 localities). Orkney voles belonged to the same phylogenetic lineage, 'Western', as individuals from France and Spain indicating southwestern Europe as the most likely source area for the islands. This result is of interest with respect to the movement and trading links of the Neolithic people who likely transported the voles. As well as the Western lineage, our phylogenetic trees revealed three other purely European lineages: the 'Italian' (single specimen from N. Italy), the 'Central' (Germany, Netherlands, Denmark) and the 'Eastern' (Hungary, Slovakia, Poland, Ukraine, Finland, European Russia). Individuals from European Russia, W. Siberia, Georgia, Ukraine and Armenia formed a fifth distinct lineage coinciding with the distribution of the 'obscurus' chromosomal form of M. arvalis. These phylogeographical data suggest that M. arvalis occupied multiple refugia during the last glaciation.     

Isolation of members of the Haemophilus-Pasteurella-Actinobacillus group from feral rodents

46 feral rodents, including a common vole (Microtus arvalis), house mice (Mus musculus), muskrats (ondatra zibetica), house rats (Rattus rattus) and brown rats (R. norvegicus) were examined for bacteria of the Haemophilus-Pasteurella-Actinobacillus group. Haemophilus spp. (only M. musculus examined) were not obtained. All animal species were found contaminated by P. pneumotropica and/or Actinobacillus spp. Almost all M. musculus (96%) and most Rattus spp. (76%) were contaminated by P. pneumotropica and/or Actinobacillus spp. These bacteria were obtained most frequently from the upper respiratory tract, to a lesser extent from the lung and rarely from caecal contents. It is concluded that feral rodents might constitute an important source of contamination of laboratory rodents by members of the HPA-group.     

Numerical and dietary responses of a predator community in a temperate zone of Europe

The generalist predation hypothesis predicts that the functional responses of generalist predator species should be quicker than those of specialist predators and have a regulating effect on vole populations. New interpretations of their role in temperate ecosystems have, however, reactivated a debate suggesting generalist predators may have a destabilizing effect under certain conditions (e.g. landscape homogeneity, low prey diversity, temporary dominance of 1 prey species associated with a high degree of dietary specialization). We studied a rich predator community dominated by generalist carnivores ( Martes spp., Vulpes vulpes, Felis catus ) over a 6 yr period in farmland and woodland in France. The most frequent prey were small rodents (mostly Microtus arvalis , a grassland species, and Apodemus spp., a woodland species). Alternative prey were diverse and dominated by lagomorphs ( Oryctolagus cuniculus, Lepus europeus ). We detected a numerical response among specialist carnivores but not among generalist predators. The dietary responses of generalist predators were fairly complex and most often dependent on variation in density of at least 1 prey species. These results support the generalist predation hypothesis. We document a switch to alternative prey, an increase of diet diversity, and a decrease of diet overlap between small and medium-sized generalists during the low density phase of M. arvalis . In this ecosystem, the high density phases of small mammal species are synchronous and cause a temporary specializing of several generalist predator species. This rapid functional response may indicate the predominant role of generalists in low amplitude population cycles of voles observed in some temperate areas.     

光照对棕色田鼠和昆明小鼠活动性的影响

光照对啮齿动物的行为格局和活动节律有着重要的影响。本研究以比较生物学方法,以光照强度和鼠种两个因素,在实验室内利用动物行为监视系统,以焦点动物取样法( Focus animal sampling) ,在＜ 20 Lux、200 Lux、800 Lux 和1 600 Lux 等4 个水平的光照强度下,监测和记录棕色田鼠和昆明小鼠的移动和静止行为,并在实验结束时测定实验动物的体重; 在800 Lux 光照强度下,设置正常( 12L∶ 12D) 和全黑( 0L∶ 24D) 两种光照时间,连续12 h监测并记录实验动物的行为。采用双因素方差分析方法对数据进行统计分析。结果表明:1) 光强与鼠种对静止行为存在显著交互作用,棕色田鼠的静止行为与光强间存在显著的负相关关系,而昆明小鼠的静止行为则与光强无显著的相关; 2) 光强对两种动物移动行为的影响与静止行为表现方式相反; 3) 在12 h的光暴露条件下,棕色田鼠的相对活动显著强于昆明小鼠; 4) 光强对两种动物体重的影响不同,棕色田鼠体重与光强呈正相关关系,昆明小鼠与光强呈负相关关系,但差异不显著。本研究进一步验证了地面鼠与地下鼠对光强适应的差别。     

Delayed dispersal in the Zaisan mole vole (Ellobius tancrei): helping or extended parental investment?

The highly social subterranean voles of genus Ellobius (mole vole) represent a unique model to compare with both social bathyergids and surface-dwelling voles. Unlike most arvicolines, mole voles display the prolonged obligatory delay of dispersal. In subterranean rodents, this delay may be associated with benefits of cooperation (weaned offspring help their parents), an extended parental investment (parents care for weaned offspring), or both. To identify the role offspring aged <3 months play in mole vole families, we estimated their contribution to important group activities. We found that juveniles contributed very little to daily living activities up to the age of approximately 2 months. The older offspring carried objects at least as frequently as breeders, but they engaged in gnawing obstacles less frequently than their fathers. Male breeders and non-breeders engaged in gnawing more than the respective categories of females. Although young mole voles clearly did not surpass their parents in performing the more energetically costly activities, they gained body mass by 26 g (130 %) between days 30 and 90, often surpassing their parents in weight. Based on our results, in E. tancrei an extremely prolonged infancy is followed by intensive building of body reserves. This ontogenetic trajectory appears to be distinct from the patterns described for social bathyergids and for most voles.     

The hair of the common hare (Lepus europaeus Pall.) and of the common vole (Microtus arvalis Pall.) as indicator of the environmental pollution

We made the INAA of hair of the common hare (Lepus europaeus Pall.) and of the common vole (Microtus arvalis Pall.) living in the emission zones. Both the hare and the vole are almost exclusively herbivores; they consume relatively large amounts of contaminated food and mirror reliably the contamination degree of the respective ecosystem. The use of free-living animals for the control of the environmental quality may complete effectively the information obtained by examination of habitants. Though the free-living animals lead a rather different way of existence it has been found that the analyses of their hair correlate very well with the analyses of human hair. It may be expected that the changes of concentrations of heavy metals will manifest themselves earlier in animals than in men, because the animals are strictly tied to the local food sources. The hair samples of hares contained increased concentrations of Sm, La, Au, As, Se, Cr, Sc, Fe, Ce, Th and Co. The hair of voles showed increased concentrations of Sm, La, Zn, As, Se, Cr, Sc, Fe, Sb, Ce, Cs and Co. A conspicuous trend towards the cumulation in hair was observed in the following elements: As, Se, Sc and Fe. The increase of their concentrations in the hair of animals from the emission regions amounted as such as to 10(3)%.     

Findings of mycobacteria in insectivores and small rodents

The organs of 30 insectivorous mammals and 62 rodents from areas inhabited by people or livestock where cattle paratuberculosis or mycobacterial infections of swine had been found to occur were examined by cultivation during the monitoring of occurrence and spread of mycobacterioses in cattle and swine. Mycobacteria were found in the organs of 3 insectivores (10%) and 6 rodents (9.7%). Mycobacterium chelonae was isolated from the organs of the lesser white-toothed shrew (Crocidura suaveolens) and the common vole (Microtus arvalis), and M. vaccae and M. avium subsp. avium (IS901+, serotype 1) from the organs of the common shrew (Sorex araneus). M. avium subsp. avium (IS901+, serotype 1) was also isolated from the organs of the yellow-necked mouse (Apodemus flavicollis). Slow-growing mycobacteria of group III (according to Runyon) were isolated from the organs of the mouse (Mus musculus sensu lato) and the yellow-necked mouse (A. flavicollis). These findings had no connection with the epizootological situation in the nearby livestock. M. fortuitum was isolated from the organs of the common vole (M. arvalis) caught in a field within easy reach of a swine breeding herd. M. fortuitum was also identified in the lymph nodes and droppings of this swine herd, as well as in the straw, scrapings from the floor of stalls, troughs and banisters, as well as from larvae and imagoes of dipterous insects. These results demonstrate the possibility that insectivores and small rodents can spread the causative agents of mycobacteria in wild and domestic animals.     

The ear in subterranean insectivora and rodentia in comparison with ground-dwelling representatives. I. Sound conducting system of the middle ear.

Compared to acoustically unspecialized mammals (soricids and murids), the middle ear of subterranean insectivores and rodents (twelve species of six families examined) was clearly distinguished and characterized by many common features: rather round and relatively larger eardrum without a pars flaccida; reduced gonial; loose or no connection between the malleus and the tympanic bone; reduced and straightened transversal part of the malleus; enlarged incus; increased and rather flat incudo-mallear joint; rather parallel position of the mallear manubrium and incudal crus longum in some species (and their fusion in bathyergids); reduced or even missing middle ear muscles. Convergent occurrence of these structural features in taxa of different origin and their generally derived character suggest that they cannot be categorized as degenerative. The form of the stapes can be considered as a non-adaptive trait; it was taxon specific yet remarkably polymorphous in some species and exhibited no convergent features among subterranean mammals. Structural retrogression resulting in a columella-like stapes was observed in some species lacking the stapedial artery. The stapedial base was relatively larger than in unspecialized mammals. The subterranean mammals did not exhibit conspicuously enlarged eardrums as would be required for sensitive tuning to low frequencies. It is, however, argued that while selective pressures in the subterranean ecotope promoted hearing of low frequencies, hearing sensitivity did not have to be enhanced.