Subterranean Rodent Research Articles

Patterns of variation in the tympanic bulla of tuco-tucos (Rodentia, Ctenomyidae, Ctenomys)

As subterranean rodents live in burrows and are constrained by the physics of their environment to vocalize, mainly in low frequencies, their expanded middle ear cavities are associated with enhanced lower-frequency hearing. Previous literature has widely acknowledged inflated tympanic bulla as a character to be found in the majority of the Ctenomys species. To explore the morphology of Ctenomys tympanic bulla, we studied a sample of 669 skulls, obtained from 21 species, for tympanic bulla size, volume, and internal structure. The study determined that bullar inflation does not seem to be the rule in Ctenomys and that the relationship between bullar size (volume) and skull size do not correspond to the phylogeny based on cytochrome b sequences thus probably being a species-specific adaptive characteristic. We also found that the internal bullar structure differs between taxa, depending on the relative contributions of cancellous (alveolar) and septate patterns to the partitioning of the bulla.

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.

Role of maternal odors on foraging behavior during postnatal development in a solitary subterranean rodent Ctenomys talarum

We investigated the role of maternal odors emanating from excretory deposits and/or glandular secretions during the postnatal development of foraging and related behaviors in young Los Talas’ tuco-tucos (Ctenomys talarum), a solitary rodent, under seminatural conditions. During cafeteria tests, we offered them two of the grasses most preferred by adults of this species (bromegrass, Bromus unioloides and panicgrass, Panicum racemosum). We scent marked one dietary option in a treatment group, and the other option in a second treatment group, keeping a third group with no odors as control. Pups did not show to prefer a special grass in particular, and maternal odors showed no effect on the behavioral variables evaluated in this study. When they reached their weaning age, they showed an ontogenetic change in food preferences, where they preferred bromegrass, and maternal odors influenced negatively on the consumption of panicgrass. During dispersal, preference for bromegrass was expressed independently of the presence of maternal odors. Overall, their effect was less pronounced than age’s effect, and it was evident in only a subset of the conducted experiments. This study shows that the influence of maternal odors is not essential for the establishment of feeding or site preferences in this species in seminatural conditions, contrarily to what was observed in other studies performed with social mammal species (i.e., rats and rabbits). It is suggested that other factors (e.g., individual learning) might influence the observed preferences.

Mitochondrial genome of Plateau zokor Myospalax baileyi

Plateau zokors Myospalax baileyi are subterranean rodents and endemic to the cold and hypoxic (2800–4300 m above sea level) climate of the farm, prairie, alpine prairie, and meadow habitats across the Tibetan plateau. The complete mitochondrial (mt) genome of M. baileyi has been determined. Our results showed that the total length of the mitogenome was 16,351 bp, and had a gene content of 13 protein coding, 22 tRNAs and 2 rRNAs. Except for the seven tRNA and Nd6 genes, all other mt genes are encoded on the heavy strand. The overall base composition of the heavy strand is 33.65% A, 29.65% T, 24.42% C, and 12.28% G, with an AT content of 63.3%.

Ecological characteristics in habitats of twoAfrican mole‐rat species with different social systems in an area of sympatry: implications for the mole‐rat social evolution

AbstractAfrican mole‐rats (Bathyergidae) are subterranean rodents with diverse social systems, which range from solitary to highly cooperative. The social systems are thought to reflect ecological conditions. We examined ecological characteristics in habitats occupied by two mole‐rat species with different social systems in an area of sympatry in theNyikaPlateau,Malawi. Whereas the solitary silvery mole‐ratHeliophobius argenteocinereusoccurs there in the afromontane grasslands, the socialWhyte's mole‐ratFukomys whyteiis bound to theMiombo woodlands. The habitat ofF. whyteiwas characterized by a lower food supply and harder soil. We suppose that the niche segregation of the two species in theNyikaPlateau is due to the inability of the solitary species to survive under the harsh ecological conditions. Absence ofF. whyteiin higher altitudes may be due to its less effective thermoregulation, competitive exclusion byH. argenteocinereus, or other unknown factors. Analysis of available data on food supply and precipitation from different mole‐rat localities revealed that there is no clear separation of the localities inhabited by solitary, social and so‐called eusocial species.

Validation of a radioimmunoassay for measuring testosterone concentrations in plasma samples of the subterranean rodent Ctenomys talarum: outstandingly elevated levels in the wild and the effect of captivity

We validated the Coat-a-Count radioimmunoassay (RIA) kit for measuring testosterone in plasma samples of the subterranean rodent Ctenomys talarum and evaluated testosterone levels in free-living and captive individuals. The performance of the assay was evaluated by the assessment of parallelism, accuracy and precision. Moreover, the high specificity of the assay antibody was confirmed by high-pressure liquid chromatography with ultraviolet detector, followed by electrospray ionization tandem mass spectrometry. Results indicated that plasma samples have to be treated with heat and diluted before the RIA for the optimization of the assay. Plasma testosterone concentrations in free-living animals were outstandingly elevated (up to 329 ng/mL), which are among the highest ever reported for mammals. On the other hand, captivity produced a 14-fold decrease in plasma testosterone concentrations, emphasizing that very significant changes in the endocrine milieu may occur in wild animals kept under laboratory conditions. Our results place tuco-tucos as an interesting model for the study of androgen regulation in mammals, suggesting that target tissues may have low sensitivity to the testosterone signal and agree with a scenario of elevated levels of sex hormone-binding globulin in plasma.

Plateau zokors on the Qinghai-Tibetan Plateau follow Bergmann's rule latitudinally, but not altitudinally

Since the first description of the Bergmann's rule, body size clines along environmental gradients have been examined in a wide variety of taxa. Broad support for Bergmann's rule has been found for endotherms and even ectotherms; many species, however, do not follow Bergmann's rule or the converse to Bergmann's rule. We tested the relationship between body size (body weight (BW), body length (BL), and 12 skull size measurements) of a typical subterranean rodent plateau zokor (Eospalax baileyi) collected from different geographic localities and two geographic variables (latitude and altitude) as well as some environmental factors that usually change with geographical gradients on the Qinghai-Tibetan Plateau. A total of 523 (212 males and 311 females) adult individuals from 21 sampling sites were analyzed. The results indicated that body size of both males and females was positively correlated with latitude, annual temperature (AT), and annual net primary production (ANPP) and negatively correlated with altitude and annual precipitation (AP). These results indicated that the plateau zokor latitudinally followed Bergmann's rule but altitudinally followed the converse to Bergmann's rule. The environmental factors which may influence the zokors’ water balance and food availability were the major driving forces latitudinally and altitudinally shaping the body size of this species, respectively.

Sleep and Wake in Rhythmic versus Arrhythmic Chronotypes of a Microphthalmic Species of African Mole Rat (Fukomys mechowii)

The giant Zambian mole rat (Fukomys mechowii) is a subterranean Afrotropical rodent noted for its regressed visual system and unusual patterns of circadian rhythmicity – within this species some individuals exhibit distinct regular circadian patterns of locomotor activity while others have arrhythmic circadian patterns. The current study was aimed at understanding whether differences in circadian chronotypes in this species affect the patterns and proportions of the different phases of the sleep-wake cycle. Physiological parameters of sleep (electroencephalogram and electromyogram) and behaviour (video recording) were recorded continuously for 72 h from 6 mole rats (3 rhythmic and 3 arrhythmic) using a telemetric system and a low-light CCTV camera connected to a DVD recorder. The results indicate that the arrhythmic individuals spend more time in waking with a longer average duration of a waking episode, less time in non-rapid eye movement (NREM) with a shorter average duration of an NREM episode though a greater NREM sleep intensity, and similar sleep cycle lengths. The time spent in rapid eye movement (REM) and the average duration of an REM episode were similar between the chronotypes.

Dispersal of arbuscular mycorrhizal fungi and dark septate endophytes by Ctenomys cf. knighti (Rodentia) in the northern Monte Desert of Argentina

In arid and semi-arid environments, root-associated fungi may play a key role in plant communities (e.g., seedling establishment, nutrient acquisition, plant survival and heat tolerance). Several studies have shown the importance of small mammals as consumers and dispersal agents of mycorrhizal fungi spores in tropical and temperate ecosystems. However, little is known about the dispersal of infective propagules of endophytic fungi in arid and semi-arid ecosystems. This study analyzed the potential role of the subterranean rodent Ctenomys cf . knighti as a dispersal agent of root-associated fungi. In order to demonstrate this role, we analyzed: (1) the incidence of colonization of arbuscular mycorrhizae and dark septate endophytes on representative plant species of the Monte Desert; (2) the presence of fungal structures of arbuscular mycorrhizae and dark septate endophytes in C. cf. knighti fecal samples; and (3) the infectivity of the fungal propagules contained in the scat and their growth effects on nine native plant species. Data strongly suggest that this South American subterranean rodent may play a key role as a dispersal agent of arbuscular mycorrhizae and dark septate endophytes fungi in the arid environment of the northern Monte Desert of Argentina.

The evolution of mitochondrial genomes in subterranean caviomorph rodents: Adaptation against a background of purifying selection

South American tuco-tucos (Ctenomys) and the related coruro (Spalacopus) are two rodent lineages that have independently colonised the subterranean niche. The energetically demanding lifestyles of these species, coupled with the hypoxic atmospheres characteristic of subterranean environments, may have altered the selective regimes on genes encoding proteins related to cellular respiration. Here, we examined the molecular evolution of 13 protein-coding genes in the mitochondrial genome of seven caviomorph rodents, including these two subterranean genera and their above-ground relatives. Using maximum-likelihood and Bayesian approaches, we estimated rates of synonymous (dS) and nonsynonymous (dN) substitutions. We found a significantly higher ω ratio (dN/dS) in subterranean groups as compared to their non-subterranean counterparts in 11 of 13 genes, although no ω ratio was larger than 1. Additionally, we applied a method based on quantitative physicochemical properties to test for positive selection. Amino acid changes implicated in radical structural or functional shifts in the protein property were found to be ubiquitous across the phylogeny, but concentrated in the subterranean lineages. Convergent changes were also found between the subterranean genera used in this study and other mammals adapted to hypoxia. The results of this study suggest a link between niche shifts and weak directional (or episodic) selection at the molecular level against a background of purifying selection.

Searching for Major Urinary Proteins (MUPs) as Chemosignals in Urine of Subterranean Rodents

Chemosensory information mediates behavior in many rodent genera. Major Urinary Proteins (MUPs) facilitate chemical communication in some species of mice. We sought to demonstrate the importance of MUPs in chemosignaling across a range of rodent genera that live in different habitats and social structures. We analyzed urine from three subterranean rodent genera from different continents, and with diverse social systems: eusocial Zambian mole-rats (Fukomys), solitary Israeli blind mole rats (Spalax), and social Chilean coruros (Spalacopus). 2D gel electrophoresis revealed low levels of protein, with sequences similar to aphrodisin, in Fukomys mole-rat urine, but no MUPs in urine of any of the studied species. Previous research demonstrated that subjects from the tested genera responded differentially to odors indicating transmission of individuality, family/colony or population, species, and reproductive state in secretions and excretions of conspecifics. This extends, to subterranean rodents, the evidence that rodent species can successfully transmit and receive chemosignals without the necessity of MUPs.

MHC variation, multiple simultaneous infections and physiological condition in the subterranean rodent Ctenomys talarum

Parasites and pathogens can play a significant role in shaping the genetic diversity of host populations, particularly at genes associated with host immune response. To explore this relationship in a natural population of vertebrates, we characterized Major Histocompatibility Complex (MHC) variation in the subterranean rodent Ctenomys talarum (the talas tuco-tuco) as a function of parasite load and ability to mount an adaptive immune response against a novel antigen. Specifically, we quantified genotypic diversity at the MHC class II DRB locus in relation to (1) natural variation in infection by multiple genera of parasites (potential agents of selection on MHC genes) and (2) antibody production in response to injection with sheep red blood cells (a measure of immunocompetence). Data were analyzed using co-inertia multivariate statistics, with epidemiological proxies for individual condition (hematocrit, leukocyte profile, body weight) and risk of parasite exposure (season of capture, sex). A significant excess of DRB heterozygotes was evident in the study population. Co-inertia analyses revealed significant associations between specific DRB alleles and both parasite load and intensity of humoral immune response against sheep red blood cells. The presence of specific DRB aminoacid sequences appeared to be more strongly associated with parasite load and response to a novel antigen than was heterozygosity at the DRB locus. These data suggest a role for parasite-driven balancing selection in maintaining MHC variation in natural populations of C. talarum. At the same time, these findings underscore the importance of using diverse parameters to study interactions among physiological conditions, immunocompetence, and MHC diversity in free-living animals that are confronted with multiple simultaneous immune challenges.

The roots of defense: plant resistance and tolerance to belowground herbivory.

BackgroundThere is conclusive evidence that there are fitness costs of plant defense and that herbivores can drive selection for defense. However, most work has focused on above-ground interactions, even though belowground herbivory may have greater impacts on individual plants than above-ground herbivory. Given the role of belowground plant structures in resource acquisition and storage, research on belowground herbivores has much to contribute to theories on the evolution of plant defense. Pocket gophers (Geomyidae) provide an excellent opportunity to study root herbivory. These subterranean rodents spend their entire lives belowground and specialize on consuming belowground plant parts.Methodology and Principal FindingsWe compared the root defenses of native forbs from mainland populations (with a history of gopher herbivory) to island populations (free from gophers for up to 500,000 years). Defense includes both resistance against herbivores and tolerance of herbivore damage. We used three approaches to compare these traits in island and mainland populations of two native California forbs: 1) Eschscholzia californica populations were assayed to compare alkaloid deterrents, 2) captive gophers were used to test the palatability of E. californica roots and 3) simulated root herbivory assessed tolerance to root damage in Deinandra fasciculata and E. californica. Mainland forms of E. californica contained 2.5 times greater concentration of alkaloids and were less palatable to gophers than island forms. Mainland forms of D. fasciculata and, to a lesser extent, E. californica were also more tolerant of root damage than island conspecifics. Interestingly, undamaged island individuals of D. fasciculata produced significantly more fruit than either damaged or undamaged mainland individuals.Conclusions and SignificanceThese results suggest that mainland plants are effective at deterring and tolerating pocket gopher herbivory. Results also suggest that both forms of defense are costly to fitness and thus reduced in the absence of the putative target herbivore.

Bite force and jaw biomechanics in the subterranean rodent Talas tuco-tuco (Ctenomys talarum) (Caviomorpha: Octodontoidea)

The Talas tuco-tuco ( Ctenomys talarum Thomas, 1898) is a South American subterranean rodent that digs using both forelimbs and incisors, the latter being used when animals face hard soils and fibrous roots. In this rodent, the incisors are also used during intermale competition for mates. Bite forces were measured on wild females (n = 21) and males (n = 21) (both adult and young individuals) using a force transducer. Bite force was significantly higher in adult males than in females (32 vs. 27 N, respectively). Bite forces calculated on the physiological cross-section of jaw adductor muscles in dissected specimens were slightly higher than in vivo measurements. Regressions against body mass showed that bite force scaled with positive allometry, with slopes of 0.89 (females) and 0.99 (males). No significant differences were observed, neither in the slope nor in the y intercept of both sexes’ equations; therefore intersexual differences in bite forces observed in adults should mainly be due to size dimorphism. Considering that soil hardness of C. talarum’s typical habitat averages 100 N/cm2, and taking into account incisor’s cross-section, it was assessed that the pressure exerted by jaw adductor muscles at the incisors level is three times higher than that required for soil penetration.

Characterization of paternity relationships in the mole rat Spalax ehrenbergi by microsatellite genotyping

AbstractSpalax ehrenbergi is a species complex of blind subterranean rodents distributed along the east Mediterranean region. We studied genetic relationships within and between S. ehrenbergi sib families using microsatellite genotyping. The upper‐bound level of multiple‐paternity rate in litters was estimated using a simulation model of breeding process. Our results show that the upper bound of multiple paternity in the studied population of S. ehrenbergi is <30% (P value 2.9%), with no detected cases of multiple paternity. Our analytical model was specifically designed for a situation in which the sibling identities are known but genetic data about their parents is unavailable. The genetic similarities between groups of individuals were also tested, and it was found that the distance between breeding nests is a factor influencing the genetic similarity between litters found in the nests.

Adaptive evolution of flaky thumb claw and elongated compulsory arousal duration in the subterranean rodent plateau zokor

The opportunities and challenges that life underground poses have led to remarkable examples of adaptive evolution in subterranean species. Here, we report two amazing specialised adaptations in a typical subterranean species, plateau zokor (Eospalax baileyi): (1) the flaky thumb claw, which facilitates the holding and cleaning of vegetation roots in the dark; and (2) largely elongated compulsory arousal duration from deep sleep, which may affect its safety in the subterranean niche. To our knowledge this is the first report of these adaptations relevant to specialisations of underground species. We propose that these findings will provide valuable information for further understanding of the developmental mechanisms involved in patterning distal limb appendages as well as sleep physiology.

Intra- and interspecific variation in home-range size in sympatric tuco-tucos, Ctenomys australis and C. talarum

Despite the fundamental nature of the home range to the biology of a species, aspects of its size, shape, and structure are not well defined in certain groups, such as subterranean rodents. These rodents, characterized by limited individual mobility and a patchy distribution of local populations, generally defend multipurpose territories in which breeding and foraging take place, increasing the chances for trade-offs among factors of habitat quality. The present study assessed the home-range size and shape of 2 species of tuco-tucos, Ctenomys australis (300–600 g) and C. talarum (100–180 g), using radiotelemetry in an area where they occur in sympatry, and explored the factors that could influence space use in these subterranean rodents. Home-range size (95% adaptive kernel) of C. australis (1,282.22 6 1,014.83 m 2 ) was ,19-fold larger than that of C. talarum (66.69 6 22.34 m 2 ). The area covered daily by C. australis represented only about 9% of the total home-range size estimated by radiotelemetry in this study and was almost twice as large as that of C. talarum, but the area covered by the latter species represented an average of 35% of its total home-range size. Total aerial and subterranean plant biomass, plant cover, and soil hardness were significantly higher in the habitat occupied by C. talarum. Contrary to expectation, body size was not the predominant factor explaining intra- and interspecific variation in home-range size. We discuss how variation in food availability in space and time and differences in the intensity of polygyny could be more important factors shaping home-range size in this genus of subterranean rodents. DOI: 10.1644/10-MAMM-A-057.1.

Ontogenetic trajectories of key morphofunctional cranial traits in South American subterranean ctenomyid rodents

Ontogenetic allometries of craniomandibular and dental features linked to digging were analyzed in 5 species of the South American subterranean rodent Ctenomys (tuco-tucos). With the exception of upper incisor procumbency, variables showed high correlation with overall skull size. In particular, craniomandibular variables related to the production of bite forces at the incisors showed near-geometric similarity during postnatal growth and interspecific changes in early developmental stages resulting in different starting forms (lateral transposition). Such an interspecific pattern of change is similar to one previously reported to occur among living and extinct ctenomyid genera. These results suggest more evolutionary flexibility for changes in early ontogenetic stages and allow rejection of the hypothesis that interspecific shape differences in the skull of Ctenomys would be associated with differences in size alone.

Digestive flexibility in females of the subterranean rodent ctenomys talarum in their natural habitat

We studied the occurrence of digestive strategies at different levels in females of the subterranean herbivorous rodent Ctenomys talarum living in their natural habitat. We determined the dimensions of different parts of the gastrointestinal tract and organs along as the activity of key digestive enzymes(sucrase, maltase and N-aminopeptidase) in small intestine in females seasonally caught. Females of C. talarum did not show seasonal variations in the mass of the different parts of the gastrointestinal tract. In nonreproductive females large intestine was longer in autumn, whereas reproductive females did not show seasonal variations in the length of the different parts of the gut. Females of C. talarum exhibited a high sucrose, maltase and N-aminopeptidase activity in small intestine, although these activities were higher in small intestine of females caught in autumn (nonreproductive) than in females caught in winter (reproductive). The results show that C. talarum females exhibit characteristics in the gut at the morphological and biochemical level, which could represent digestive strategies to face the constraints imposed by their costly particular way of life.

Morphological adaptations of incisors in the subterranean Gansu zokor, Myospalax cansus (Rodentia, Spalacidae)

The incisor morphology of rodents varies a good deal among different genera and each structure may have a special evolutionary significance. Some basic and lateral profile measurements of upper and lower incisors which may reflect morphological adaptations of the Gansu zokor (Myospalax cansus, a typical subterranean rodent in northern Asia) and the brown rat (Rattus norvegicus, a typical aboveground rodent that has close body size to the Gansu zokor) were analyzed. GIS (Geographic Information System) software and nonlinear regression were used to analyze incisor lateral profile, allowing the incisors to be viewed as circular arcs with a high degree of accuracy. The results show that: i) zokors have more robust (i.e. larger anteroposterior diameter and transverse diameter values), heavier and longer upper as well as lower incisors than rats; ii) zokors show a significantly higher level of sexual dimorphism (male dominant) than rats on the incisor morphology (including basic and lateral profile measurements) and iii) the upper incisor is heavier than lower incisor in rats, as opposed to zokors, in which the lower incisor is heavier than the upper incisor, indicating that more resources must have been allocated to lower incisors of zokors.