Subterranean Rodent Species Research Articles

CDNA cloning and expression of erythropoietin in the plateau zokor (Myospalax baileyi) from the Qinghai-Tibet Plateau

All organisms respond to variation in their environments and manage environmental stress through metabolic adjustments. The plateau zokor (Myospalax baileyi) is an endemic and keystone subterranean rodent species that inhabits the Qinghai-Tibet Plateau between 2800 and 4200 m above sea level. It is a hypoxic-tolerant mammal with a high ratio of oxygen utilization that enables it to cope with its harsh surroundings. To explore the molecular mechanism of altitude acclimatization of the plateau zokor, we cloned the zokor erythropoietin (Epo) gene and used real-time PCR to compare Epo mRNA levels in zokors inhabiting 16 different altitudes. The full-length zokor Epo open reading frame was 579 bp that encoded a precursor peptide of 192 amino acids with a signal peptide of 26 residues. The Epo gene of the plateau zokor was 81%-95% homologous to that of human, mouse, rat, root vole and the Golan Heights blind mole rat, with the highest homology (95%) to species of the genus Spalax. Epo mRNA was detected mainly in the zokor kidney and spleen among 8 selected tissues. The level of Epo mRNA increased in the liver and kidney with increases in altitude. The increase in the kidney was 5 times that in the liver. Remarkably, expression of Epo mRNA in the kidney of zokors living at the highest altitude (4268 m) was 12-fold higher than that of zokors living at the lowest (2492 m) altitude. These findings provide essential information for understanding the possible role of Epo in adaptation to hypoxia in the plateau zokor.

Genetic variation over 10 000 years in Ctenomys: comparative phylochronology provides a temporal perspective on rarity, environmental change and demography

An understanding of how ecological traits influence past species response to environmental change can aid our future predictions of species persistence. We used ancient DNA and serial coalescent modelling in a hypothesis-testing framework to reveal differences in temporal genetic variation over 10,000 years for two species of subterranean rodents that currently differ in rarity (abundance, range size and habitat specificity) and mating system, but that reside in the same volcanically active region. Comparative phylochronologic analyses indicated little genetic change and suggest genetic stability in the solitary widespread Ctenomys haigi over thousands of years. In contrast, we found a pattern of haplotypic turnover in the rare and currently endangered Ctenomys sociabilis. Serial coalescent modelling indicated that the best-fit models of microevolutionary change included gene flow between isolated populations for this species. Although C. haigi and C. sociabilis are congeners that share many life history traits, they have behavioural, habitat-preference and population-size differences that may have resulted in contrasting patterns of temporal variation during periods of environmental change.

PHOTIC INDUCTION OF Fos IN THE SUPRACHIASMATIC NUCLEUS OF AFRICAN MOLE-RATS: RESPONSES TO INCREASING IRRADIANCE

African mole-rats (family Bathyergidae) are strictly subterranean rodent species that are rarely exposed to environmental light. Morphological and physiological adaptations to the underground environment include a severely reduced eye size and regressed visual system. Responses of the circadian system to light, however, appear to be intact, since mole-rats are able to entrain their circadian activity rhythms to the light-dark cycle and light induces Fos expression in the suprachiasmatic nucleus (SCN). Social organization varies from solitary species to highly elaborated eusocial structures, characterized by a distinct division of labor and in which one reproductive female regulates the behavior and reproductive physiology of other individuals in the colony. The authors studied light-induced Fos expression in the SCN to increasing light intensities in four mole-rat species, ranging from strictly solitary to highly social. In the solitary Cape mole-rat, light induces significant Fos expression in the SCN, and the number of Fos-immunopositive cells increases with increasing light intensity. In contrast, Fos induction in the SCN of social species was slightly greater than, but not statistically different from, the dark-control animals as is typical of most rodents. One species showed a trend for an increase in expression with increased light, whereas a second species showed no trend in expression. In the naked mole-rat, Fos expression appeared higher in the dark-controls than in the animals exposed to light, although the differences in Fos expression were not significant. These results suggest a gradient in the sensitivity of the circadian system to light in mole-rats, with a higher percentage of individuals that are unresponsive to light in correlation with the degree of sociality. In highly social species, such as the naked mole-rat that live in a relatively stable subterranean milieu in terms of food availability, temperature, constant darkness, and devoid of 24-h cyclic environmental cues, the temporal coordination of rest-wake activities may be dependent on social interactions and social status rather than on photic regulation of the circadian timing system. (Author correspondence: moosthuizen@zoology.up.ac.za)

Retinal photoreceptors of two subterranean tuco‐tuco species (Rodentia, Ctenomys): Morphology, topography, and spectral sensitivity

Traditionally, vision was thought to be useless for animals living in dark underground habitats, but recent studies in a range of subterranean rodent species have shown a large diversity of eye features, from small subcutaneous eyes to normal-sized functional eyes. We analyzed the retinal photoreceptors in the subterranean hystricomorph rodents Ctenomys talarum and Ctenomys magellanicus to elucidate whether adaptation was to their near-lightless burrows or rather to their occasional diurnal surface activity. Both species had normally developed eyes. Overall photoreceptor densities were comparatively low (95,000-150,000/mm(2) in C. magellanicus, 110,000-200,000/mm(2) in C. talarum), and cone proportions were rather high (10-31% and 14-31%, respectively). The majority of cones expressed the middle-to-longwave-sensitive (L) opsin, and a 6-16% minority expressed the shortwave-sensitive (S) opsin. In both species the densities of L and S cones were higher in ventral than in dorsal retina. In both species the tuning-relevant amino acids of the S opsin indicate sensitivity in the near UV rather than the blue/violet range. Photopic spectral electroretinograms were recorded. Unexpectedly, their sensitivity profiles were best fitted by the linear summation of three visual pigment templates with lambda(max) at 370 nm (S pigment, UV), at 510 nm (L pigment), and at 450 nm (an as-yet unexplained mechanism). Avoiding predators and selecting food during the brief aboveground excursions may have exerted pressure to retain robust cone-based vision in Ctenomys. UV tuning of the S cone pigment is shared with a number of other hystricomorphs.

Parasitism underground: determinants of helminth infections in two species of subterranean rodents (Octodontidae)

Patterns of infection among hosts in a population are often driven by intrinsic host features such as age or sex, as well as by positive or negative interactions between parasite species. We investigated helminth parasitism in 2 South American rodent species, Ctenomys australis and C. talarum (Octodontidae), to determine whether the unusual solitary and subterranean nature of these hosts would impact their patterns of infection. We applied generalized linear models to infection data on a total of 7 helminth species (1 in C. australis and 6 in C. talarum). Host age and season of capture influenced infection levels in some of the helminth species, but none were influenced by host body condition. In C. talarum, 4 pairs of helminth species showed significant associations, either asymmetrical or symmetrical, and with 3 of the 4 being positive; strong inter-specific facilitation appears likely in 1 case. Also, we found that female hosts, especially non-pregnant ones, harboured heavier infections of 2 nematode species than male hosts. This is in sharp contrast to the general male-bias reported for most studies of nematodes in wild mammals, and we develop explanations for these results based on the unusual ecology of these subterranean rodents.

Ontogeny of spatial working memory in the subterranean rodentctenomys talarum

While several works analyzed the spatial learning and memory capacities in adults of subterranean rodents, no study was done examining the development of these cognitive processes in pups of any of those species. Therefore, the development of spatial working memory in the South American subterranean rodent Ctenomys talarum was investigated by analyzing the pups' spatial performance in a delayed alternation task. When a short delay of 1 min was interposed between runs in the Y-maze, 20-day-old pups made more errors than 40- and 60-day-old pups. When longer intervals (10 min) were elapsed between runs, younger pups made approximately twice as many errors as the ones committed by 60-day-old pups, showing the age-dependent development of spatial working memory in this species of subterranean rodent. Increased space use by C. talarum pups, caused first by the appearance of independent exploratory behavior and later by the need of leaving maternal territory and construct a new burrow system, showed some correspondence with the improvements in the pups' spatial working memory performance, suggesting for the importance of this cognitive capacity in developing pups for which spatial learning and memory constitute essential abilities for survival and fitness.

Dispersal and population structure at different spatial scales in the subterranean rodent Ctenomys australis

BackgroundThe population genetic structure of subterranean rodent species is strongly affected by demographic (e.g. rates of dispersal and social structure) and stochastic factors (e.g. random genetic drift among subpopulations and habitat fragmentation). In particular, gene flow estimates at different spatial scales are essential to understand genetic differentiation among populations of a species living in a highly fragmented landscape. Ctenomys australis (the sand dune tuco-tuco) is a territorial subterranean rodent that inhabits a relatively secure, permanently sealed burrow system, occurring in sand dune habitats on the coastal landscape in the south-east of Buenos Aires province, Argentina. Currently, this habitat is threatened by urban development and forestry and, therefore, the survival of this endemic species is at risk. Here, we assess population genetic structure and patterns of dispersal among individuals of this species at different spatial scales using 8 polymorphic microsatellite loci. Furthermore, we evaluate the relative importance of sex and habitat configuration in modulating the dispersal patterns at these geographical scales.ResultsOur results show that dispersal in C. australis is not restricted at regional spatial scales (~ 4 km). Assignment tests revealed significant population substructure within the study area, providing support for the presence of two subpopulations from three original sampling sites. Finally, male-biased dispersal was found in the Western side of our study area, but in the Eastern side no apparent philopatric pattern was found, suggesting that in a more continuous habitat males might move longer distances than females.ConclusionsOverall, the assignment-based approaches were able to detect population substructure at fine geographical scales. Additionally, the maintenance of a significant genetic structure at regional (~ 4 km) and small (less than 1 km) spatial scales despite apparently moderate to high levels of gene flow between local sampling sites could not be explained simply by the linear distance among them. On the whole, our results support the hypothesis that males disperse more frequently than females; however they do not provide support for strict philopatry within females.

Cost of digging is determined by intrinsic factors rather than by substrate quality in two subterranean rodent species

Searching for food by extensive digging is one of the most important aspects of life of subterranean rodents. We studied the effect of extrinsic (substrate quality) and intrinsic factors (sex and body mass) upon the cost of burrowing, expressed as digging metabolic rate (DMR) in two African mole-rat species (Bathyergidae, Rodentia) with distinct social structures. The sexually dimorphic giant mole-rat ( Fukomys mechowii) is a highly social species, whereas the almost monomorphic silvery mole-rat ( Heliophobius argenteocinereus) is a solitary bathyergid. Burrowing in F. mechowii was more costly (DMR was greater) than in H. argenteocinereus, but there was no difference in burrowing speed between both species. DMR within a particular species was dependent upon body mass, but independent of sex. Different substrate quality had no effect upon DMR in either species, yet it affected burrowing speed. We conclude that less effective digging in F. mechowii can be compensated by the joint workforce of other family members. Alternatively, H. argenteocinereus, being a more effective digger, can afford a solitary way of life.

Sound transmission and burrow characteristics of the subterranean rodentCtenomys talarum (Rodentia: Ctenomyidae)

Males of tuco-tucoCtenomys talarum Thomas, 1898 use particular burrow’s entrances to emit their territorial vocalization. Therefore we studied the internal structure of these entrances and the possible effect on the emission and propagation of airborne sounds. Externally, the burrow entrances used by tuco-tucos males to vocalize were characterized by the absence of sand mounds around their openings. Internally, most of the burrow’s entrances consisted of a main, relatively straight, tunnel of 30–40 cm length, with a diameter of 5.7–6.4 cm. After passing through the burrow’s entrance, the low-frequency components of an artificial signal played back inside the tunnel were not only less attenuated but also amplified (measured at 10–30 cm from the burrow opening). Therefore, the emission of territorial vocalizations inside the particular burrow’s entrances may be considered as a complex adaptative behavior, in which burrow structure improves the signal emission and propagation. Moreover, this work also showed thatC. talarum’s territorial vocalization seems to be adequate for long, inter-burrow communication, since its physical characteristics (high amplitude and low main frequency) are concomitant with the frequencies that are better transmitted in the natural habitat of this species of subterranean rodent.

Strongyloides myopotami in ctenomyid rodents: Transition from semi-aquatic to subterranean life cycle

AbstractStrongyloides myopotami, a parasite of Myocastor coypus (nutria or coypu), was found during an extensive parasitological survey carried out on parasitic helminths of 5 species of subterranean rodents (tuco-tucos) belonging to the genus Ctenomys from Argentina and Uruguay. Strongyloides myopotami became known by causing “marsh itch” (also called “nutria itch” or “swimmer’s itch”), a severe rash caused by larvae that enter the skin in humans, and it is recognised as a zoonosis for people handling nutria fur. In the present study S. myopotami was found in 2 of the 5 examined species of Ctenomys (C. talarum from Argentina and C. pearsoni from Uruguay), both inhabiting the vicinity of water courses. Population descriptors of S. myopotami in C. talarum showed that a population of this parasite is well established in this rodent. The development of infective filariform larvae from eggs in the faeces of C. talarum and the prevalence of gravid parasitic females in this host can be considered as evidence of the establishment of a population of S. myopotami independent of the source population parasitizing M. coypus. Therefore, the presence of S. myopotami in these species of tuco-tucos indicates a change from a semi-aquatic to subterranean life cycle. Evidence that tuco-tucos are reservoirs for these nematodes and therefore may be a risk to human health in the areas studied is provided.

Genetic diversity of the subterranean Gansu zokor in a semi‐natural landscape

AbstractWe studied the relationship between genetic diversity of the subterranean Gansu zokor Myospalax cansus and habitat variability in the Loess Plateau, Qinghai Province, China. We used a combination of geographic information systems and molecular techniques to assess the impact of habitat composition and human activities on the genetic diversity of zokor populations in this semi‐natural landscape. Although they occurred relatively infrequently in the landscape, woodland and high‐coverage grassland habitats were the main positive contributors to the genetic diversity of zokor populations. Rural residential land, plain agricultural land and low‐coverage grassland had a negative effect on genetic diversity. Hilly agricultural land and middle‐coverage grassland had little impact on zokor genetic diversity. There were also interactions between some habitat types, that is, habitat types with relatively better quality together promoted conservation of genetic diversity, while the interaction between (among) bad habitat types made situations worse. Finally, habitat diversity, measured as patch richness and Shannon's diversity index, was positively correlated with the genetic diversity. These results demonstrated that: (1) different habitat types had different effects on the genetic diversity of zokor populations and (2) habitat quality and habitat heterogeneity were important in maintaining genetic diversity. Habitat composition was closely related to land use thus emphasizing the importance of human activities on the genetic diversity of subterranean rodent populations in this semi‐natural landscape. Although the Gansu zokor was considered to be a pest species in the Loess Plateau, our study provides insights for the management and conservation of other subterranean rodent species.

Genetic structure in a solitary rodent (Ctenomys talarum): implications for kinship and dispersal

The genetic structure of a population provides critical insights into patterns of kinship and dispersal. Although genetic evidence of kin structure has been obtained for multiple species of social vertebrates, this aspect of population biology has received considerably less attention among solitary taxa in which spatial and social relationships are unlikely to be influenced by kin selection. Nevertheless, significant kin structure may occur in solitary species, particularly if ecological or life history traits limit individual vagility. To explore relationships between genetic structure, kinship, and dispersal in a solitary vertebrate, we compared patterns of genetic variation in two demographically distinct populations of the talar tuco-tuco (Ctenomys talarum), a solitary species of subterranean rodent from Buenos Aires Province, Argentina. Based on previous field studies of C. talarum at Mar de Cobo (MC) and Necochea (NC), we predicted that natal dispersal in these populations is male biased, with dispersal distances for males and females being greater at NC. Analyses of 12 microsatellite loci revealed that in both populations, kin structure was more apparent among females than among males. Between populations, kinship and genetic substructure were more pronounced at MC. Thus, our findings were consistent with predicted patterns of dispersal for these animals. Collectively, these results indicate that populations of this solitary species are characterized by significant kin structure, suggesting that, even in the absence of sociality and kin selection, the spatial distributions and movements of individuals may significantly impact patterns of genetic diversity among conspecifics.

Synaptic behaviour and morphological modifications of the X and Y chromosomes during pachytene in three species of Ctenomys (Rodentia, Caviomorpha, Ctenomyidae).

Synaptic behaviour and the progression of morphological differentiation of the XY chromosome pair during pachytene was studied for the first time in three species of the South American subterranean rodents of the genus Ctenomys (tuco-tucos). In general, synapsis progression in the sex pair could be subdivided into four substages: (i) initial partial synapsis of the X and Y chromosome axes and beginning of the differentiation of the unsynapsed regions; (ii) complete or almost complete synapsis of the Y axis accompanied with morphological differentiation of the unsynapsed region of the X chromosome; (iii) a novel stage exclusive to Ctenomys perrensi consisting in a retraction of the free X axis, associated with the formation of a homogeneous and dense structure along the synaptic region, which leads to the achievement of full synapsis between sex chromosomes; or (iv) an increase in morphological complexity involving extreme splitting of the XY pair. The implications of the peculiar synaptic behaviour displayed by sex chromosomes in C. perrensi, a species complex highly polymorphic for Robertsonian translocations, are discussed in relation to both the triggering of the pachytene checkpoint and the avoidance of non-homologous associations between sex chromosomes and the asynaptic pericentromeric regions of trivalents in translocation heterozygotes.

Acoustic signals of a solitary subterranean rodent Ctenomys talarum (Rodentia: Ctenomyidae): physical characteristics and behavioural correlates

The purpose of this study was to analyse and describe vocalizations of a solitary subterranean rodent, Ctenomys talarum. In adult C. talarum five different sounds (four true vocalizations and one mechanical sound) were recorded during different behavioural contexts. Using data from the laboratory and literature, we classified these vocalizations as territorial, distress, and mating calls. We found that the vocalization range in C. talarum is shifted towards low frequencies, which transmit better in underground burrows and match well the hearing range described for other species of subterranean rodents. These low-frequency vocalizations, also found in other non-related subterranean rodents, may reflect an adaptation to the acoustic conditions of the habitat.

Convergent evolution of the vestibular organ in the subterranean mole‐rats, Cryptomys and Spalax, as compared with the aboveground rat, Rattus

The membranous labyrinth of the vestibular organ (examined in toto) in two unrelated species of subterranean rodents, Cryptomys sp. from Zambia and Spalax ehrenbergi from Israel, was in many parameters (streamline length, curvature radius, and cross-sectional area of the lumen) relatively or even absolutely (especially the cross-sectional area) larger than in the laboratory Norway rat. The mechanical sensitivity of the vestibular organ (estimated according to the mathematical model of Oman et al., [1987] Acta. Otolaryngol (Stockh.) 103:1-13) was similar in both subterranean rodent species and significantly higher than that in the laboratory rat. The most pronounced differences in morphometry and the resulting mechanical sensitivity between the subterranean forms and the rat occurred in the lateral (i.e., phylogenetically and ontogenetically most recent and presumably most plastic) semicircular duct. The area of the sensory epithelia, and density and total numbers of vestibular receptors, were estimated on surface specimens for both maculae and for all three cristae for all three species. While the density of hair cells in comparable sensory epithelia was similar in all three species, the sensory area and thus, also, the total receptor counts were significantly larger in both subterranean forms. The peripheral vestibular organ in subterranean rodents is, in comparison to a generalized aboveground dwelling form, i.e., the rat, progressively specialized, and in any case cannot be denoted as degenerate.

Owl Predation on Two Sympatric Species of Tuco-Tucos (Rodentia: Octodontidae)

Predation by owls upon two sympatric species of subterranean rodents of the genus Ctenomys was studied by comparing characteristics of individuals that were field-trapped and preyed upon. Predators took a greater proportion of the smaller C. talarum than of the larger C. australis in comparison to that estimated from their respective field densities. Only subadult individuals of C. australis were found among pellets. For C. talarum , a greater proportion of subadults than of adults was observed in pellets. We suggest that this pattern is determined both by constraints imposed by size of prey on the ability of a predator to handle large prey and by greater exposure of dispersing subadults to predation. Differential predation possibly maintains the habitat segregation observed between C. talarum and C. australis .

Habitat Shift After Experimental Removal of the Bigger Species in Sympatric Ctenomys Talarum and Ctenomys Australis (Rodentia: Octodontidae)

AbstractA removal trapping experiment was conducted in the field to investigate if microhabitat choice and population characteristics of Ctenomys talarum are affected by the bigger, dominant Ctenomys australis, in a zone where these subterranean rodent species are geographically sympatric. As reported previously by other authors, the species were distributed in a habitat segregation pattern which characterized the initial state, prior to C. australis removal. I detected a significant habitat shift-that is, changes in microhabitat choice by C. talarum individuals- in response to C. australis removal. However, it is remarkable that this only occurred after one year of continuous removal of C. australis, and was restricted to a very small expansion by C. talarum into the fringe of the area previously occupied by the dominant species. In addition, a slight increase of the C. talarum population density took place which was possibly due to the absence of the other species. It is suggested that the microhabitat typical of C. australis (with deeper, more friable soil and less vegetation) could be suboptimal and thus unpreferred for C. talarum. If the pre-experimental C. talarum population was satiated to its carrying capacity, it is possible that the small number of C. talarum individuals-mostly subadults-had invaded areas previously occupied by C. australis because they had no other choice than a suboptimal habitat. No substantial changes were detected in other population characteristics (sex ratio, age structure, distance between individuals) which were very similar to that in a control area. Interspecific interactions and displacement by the bigger C. australis could be significant but nonetheless marginal in sustaining the pattern of microhabitat segregation between the species. Difference in habitat preference, linked with species differences in body size and colour, are probably of much greater importance.

Major histocompatibility complex of the mole-rat. I. Serological and biochemical analysis.

The mole-rat, Spalax ehrenbergi, is a complex subterranean rodent species whose habitat is restricted largely to the Middle East and North Africa. We typed over 50 mole-rats with mouse monoclonal and polyclonal antibodies specific for class I and class II major histocompatibility complex (Mhc) molecules. Some of these antibodies were produced against mouse Mhc molecules, others against Mhc molecules of other species. About 25% of the antibodies reacted with mole-rat lymphocytes in the cytotoxic test. Some of the serologically positive antibodies precipitated from a glycoprotein pool of mole-rat spleen cell molecules that corresponded in size with class I and class II molecules of other species. We conclude, therefore, that mole-rats, like other mammals, possess the Mhc which consists of class I and class II loci. We call this Mhc Spalax major histocompatibility (Smh) complex. The occurrence of a large number of different serotypes among the tested animals suggests that Smh loci are polymorphic. This Mhc polymorphism of the mole-rat contrasts with the monomorphism or oligomorphism of the Syrian hamster, a rodent with a similar ecology. Thus far no qualitative correlation could be found between Smh polymorphism and chromosome variation described in this superspecies.