Subterranean Mammals Research Articles

Subterranean Sympatry: An Investigation into Diet Using Stable Isotope Analysis

In the Western Cape three species of mole-rat occur in sympatry, however, little is known about differences in their dietary preferences. Dietary composition of the three species; the common mole-rat (Cryptomys hottentotus hottentotus), the Cape mole-rat (Georychus capensis) and the Cape dune mole-rat (Bathyergus suillus) were examined using stable isotope analysis. Blood, fur and claw samples were collected from 70 mole-rats, in addition to several potential food items, to assess food selection of the three species under natural conditions. Overall there was a significant difference in the isotopic composition (δ13C and δ15N) between all three species and significant differences in their diet composition. There were also significant differences between tissues in all three species suggesting temporal variation in diet. The small size and colonial lifestyle of C. h. hottentotus allows it to feed almost 100% on bulbs, while the solitary and larger species G. capensis and B. suillus fed to a greater extent on other resources such as grasses and clover. B. suillus, the largest of the species, had the most generalized diet. However, overall all species relied most heavily upon geophytes and consumed the same species suggesting competition for resources could exist. We also showed a high level of individual variation in diet choices. This was most pronounced in B. suillus and G. capensis and less so in C. h. hottentotus. We demonstrate that stable isotope analysis can successfully be applied to examine dietary patterns in subterranean mammals and provide insights into foraging patterns and dietary variation at both the inter and intra population level.

Cancer resistance in the blind mole rat is mediated by concerted necrotic cell death mechanism

Blind mole rats Spalax (BMR) are small subterranean rodents common in the Middle East. BMR is distinguished by its adaptations to life underground, remarkable longevity (with a maximum documented lifespan of 21 y), and resistance to cancer. Spontaneous tumors have never been observed in spalacids. To understand the mechanisms responsible for this resistance, we examined the growth of BMR fibroblasts in vitro of the species Spalax judaei and Spalax golani. BMR cells proliferated actively for 7-20 population doublings, after which the cells began secreting IFN-β, and the cultures underwent massive necrotic cell death within 3 d. The necrotic cell death phenomenon was independent of culture conditions or telomere shortening. Interestingly, this cell behavior was distinct from that observed in another long-lived and cancer-resistant African mole rat, Heterocephalus glaber, the naked mole rat in which cells display hypersensitivity to contact inhibition. Sequestration of p53 and Rb proteins using SV40 large T antigen completely rescued necrotic cell death. Our results suggest that cancer resistance of BMR is conferred by massive necrotic response to overproliferation mediated by p53 and Rb pathways, and triggered by the release of IFN-β. Thus, we have identified a unique mechanism that contributes to cancer resistance of this subterranean mammal extremely adapted to life underground.

How attractive is the girl next door? An assessment of spatial mate acquisition and paternity in the solitary Cape dune mole-rat, Bathyergus suillus.

Behavioural observations of reproduction and mate choice in wild fossorial rodents are extremely limited and consequently indirect methods are typically used to infer mating strategies. We use a combination of morphological, reproductive, spatial, and genetic data to investigate the reproductive strategy of a solitary endemic species, the Cape dune mole-rat Bathyergus suillus. These data provide the first account on the population dynamics of this species. Marked sexual dimorphism was apparent with males being both significantly larger and heavier than females. Of all females sampled 36% had previously reproduced and 12% were pregnant at the time of capture. Post-partum sex ratio was found to be significantly skewed in favour of females. The paternity of fifteen litters (n = 37) was calculated, with sires assigned to progeny using both categorical and full probability methods, and including a distance function. The maximum distance between progeny and a putative sire was determined as 2149 m with males moving between sub-populations. We suggest that above-ground movement should not be ignored in the consideration of mate acquisition behaviour of subterranean mammals. Estimated levels of multiple paternity were shown to be potentially as high as 26%, as determined using sibship and sire assignment methods. Such high levels of multiple paternity have not been found in other solitary mole-rat species. The data therefore suggest polyandry with no evidence as yet for polygyny.

Season but not sex influences burrow length and complexity in the non‐sexually dimorphic solitaryCape mole‐rat (Rodentia:Bathyergidae)

AbstractLittle is known about how season influences burrowing activity, burrow structure or reproductive behaviour in subterranean mammals. We excavated burrow systems of male and femaleGeorychus capensis, a solitary, subterranean rodent, in winter (wet season) and summer (dry season) to investigate whether, if any, seasonal differences were due to putative mate‐seeking behaviour of males. Burrow structure differed between seasons but not between sexes. For both sexes, summer burrows were shorter and covered a smaller area, but explored the surrounding environment more efficiently than winter burrows.Summer burrows had fewer mounds, which indicated that less expansion of the burrow systems occurred during this season. We discuss these differences in exploration and the use of the environment between seasons in terms of mating strategies ofG. capensisand observed levels of sexual dimorphism in our populations. This study supports recent ideas regarding sexual selection relating to exaggerated traits in females, which affect a female's ability to acquire reproductive resources that often appear similar to that selected for by males.

Influence of spatial environment on maze learning in an African mole-rat

In subterranean species where excavation is energetically expensive, efficient spatial navigation is vital to reducing the costs of locating important resources such as food and mates. While spatial navigational ability is positively correlated with sociality in subterranean mammals, we have a less clear understanding of the role of habitat complexity on navigational ability. We tested spatial navigational ability and memory in 12-18-month captive Natal mole-rats (Cryptomys hottentotus natalensis) maintained in a simple environment with no environmental enrichment and newly captured wild individuals from natural, complex burrow systems. In maze trials, mole-rats captured freshly from the wild made significantly fewer navigational errors, were more likely to successfully navigate the maze, travelled shorter distances and as a consequence, completed the maze in less time. Male mole-rats from both experimental treatments were more likely to complete the maze than females. Memory retention of the maze was tested on day two, seven, 30 and 60, respectively. The results were variable, although both groups showed a significant memory retention 60 days after testing. Our results highlight the potential importance of the environment (microhabitat complexity) on spatial cognitive performance in mole-rats.

Diet and prey selection of the southern marsupial mole: an enigma from Australia's sand deserts

AbstractThe two marsupial moles are the sole extant members of the order Notoryctemorphia, an ancient Australian lineage, with extreme adaptations for fossoriality. We tested whether the order conforms to the expectation that the low productivity of subterranean environments results in subterranean mammals being generalist feeders. To do this, we examined diet, invertebrate availability in foraging areas and prey selection by the southern marsupial mole or Itjaritjari Notoryctes typhlops, which occupies the sand deserts of southern and central Australia. Because the species is so infrequently encountered, we examined digestive tracts from museum specimens which themselves are rare; we obtained access to ∼12% of all specimens available in Australia's museums. Our invertebrate sampling protocol was based on a novel survey method, which, for the first time, enables quantification of the distribution and habitat use of N. typhlops. We sampled topographic positions on sandridges and areas of the soil profile (0–70 cm) where marsupial moles forage. Rarefaction methods indicated our sample size was sufficient to record the majority of prey items. Material in digestive tracts of 16 specimens consisted of five insect orders (Coleoptera, Hymenoptera, Isoptera, Lepidoptera and Orthoptera), scorpions, spiders and plant material. N. typhlops consumed two main prey types: social insects (ants and termites) and the larvae of beetles. Ants, termites and beetle larvae were also the main invertebrates captured in soil cores on sandridges; other invertebrates combined contributed <5% to abundance. Prey selection assessment using Jacobs' index and Bonferroni confidence intervals indicated an active avoidance of termites (D = −0.61), whereas ants (D = −0.13) and beetle larvae (D = 0.57) and all other prey categories were taken in proportion to availability. Our results show that N. typhlops is best classed as a dietary generalist despite its specialized adaptations for a subterranean lifestyle.

Teasing apart socially‐induced infertility in non‐reproductive female Damaraland mole‐rats, Fukomys damarensis (Rodentia: Bathyergidae)

The Damaraland mole-rat is a subterranean mammal exhibiting extreme reproductive skew with a single reproductive female in each colony responsible for procreation. Non-reproductive female colony members are physiologically suppressed while in the colony, exhibiting reduced concentrations of plasma luteinizing hormone (LH) and a decreased response of the pituitary, as measured by the release of bioactive LH, to an exogenous dose of gonadotrophin releasing hormone (GnRH). Removal of the reproductive female from the colony results in an elevation of LH and an enhanced response of the pituitary to a GnRH challenge in non-reproductive females comparable to reproductive females, implying control of reproduction in these individuals by the reproductive female. The Damaraland mole-rat is an ideal model for investigating the physiological and behavioral mechanisms that regulate the hypothalamo-pituitary-gonadal axis. In contrast, we know less about the control of reproduction at the level of the hypothalamus. The immunohistochemistry of the GnRH system of both reproductive and non-reproductive female Damaraland mole-rats has revealed no significant differences with respect to morphology, distribution or numbers of immunoreactive GnRH perikarya. We examined whether the endogenous opioid peptide beta-endorphin was responsible for the inhibition of the release of the GnRH from the neurons indirectly by measuring LH concentrations in these non-reproductive females following single, hourly and 8 hourly injections of the opioid antagonist naloxone. The results imply that the endogenous opioid peptide, beta-endorphin, is not responsible for the inhibition of GnRH release from the perikarya in non-reproductive females. Preliminary data examining the circulating levels of cortisol also do not support a role for circulating glucocorticoids. The possible role of kisspeptin is discussed.

Socially induced infertility in Ansell's mole‐rat: are there depressed hormone levels in non‐reproductive males and females?

AbstractAnsell's mole‐rat, Fukomys anselli, is a social subterranean mammal and exhibits an extreme reproductive division of labour. Reproduction in the colony is restricted usually to a single female. Complete colonies captured throughout an entire calendar year were euthanased and the histology of the gonads and plasma hormone concentrations were measured in reproductive and non‐reproductive members of both sexes. In males, the circulating levels of testosterone were significantly higher in the reproductive male than the non‐reproductive males. The mean testes mass for the reproductive males corrected for body mass was not significantly greater than that of the non‐reproductive male. Similarly, the mean testes volume of reproductive males was not greater than that for the non‐reproductive males but the seminiferous tubule diameter was significantly greater in the reproductive males than the non‐reproductive males. Reproductive females characteristically possessed corpora lutea of ovulation and pregnancy in their ovaries and this was met with much higher progesterone concentrations in the reproductive females 34 nmol/L compared with 4 nmols/L in the non‐reproductive females. In contrast, non‐reproductive females showed a complete range of follicular genesis, but they did not possess corpora lutea of ovulation or pregnancy, in turn they show depressed progesterone concentrations. The current evidence suggests that in Ansell's mole‐rats, the non‐reproductive males and females refrain from sexual activity by being subordinate and moreover, related to the breeding pair.

Dental anomalies in the Japanese mole Mogera wogura from northeast China and the Primorsky region of Russia

Dental anomalies in the Japanese mole, Mogera wogura Temminck, 1842, from northeast China and the Primorsky region of Russia were examined based on 241 specimens. The most frequent dental anomaly was oligodonty, i.e., missing P2 (18 cases) or P3 (one case). Supernumerary teeth were observed in three cases, two of which were characterized by abnormal shapes. Morphological abnormalities in teeth (six cases) and an asymmetrically curved rostrum (one case) were also observed. Dental anomalies were found at higher frequencies in populations near the northern range limit of the species. This was not caused by size effects. We suggest that the high incidence of dental anomalies was the result of genetic drift, which increases in marginal populations. Considering the nature of subterranean mammals, our results suggest that the high frequency of dental anomalies in a marginal population could have initiated the evolution of dental formulae if parapatric or peripatric speciation occurs in such populations.

Evolution Under Environmental Stress at Macro- and Microscales

Environmental stress has played a major role in the evolution of living organisms (Hoffman AA, Parsons PA. 1991. Evolutionary genetics and environmental stress. Oxford: Oxford University Press; Parsons PA. 2005. Environments and evolution: interactions between stress, resource inadequacy, and energetic efficiency. Biol Rev Camb Philos Soc. 80:589–610). This is reflected by the massive and background extinctions in evolutionary time (Nevo E. 1995a. Evolution and extinction. Encyclopedia of Environmental Biology. New York: Academic Press, Inc. 1:717–745). The interaction between organism and environment is central in evolution. Extinction ensues when organisms fail to change and adapt to the constantly altering abiotic and biotic stressful environmental changes as documented in the fossil record. Extreme environmental stress causes extinction but also leads to evolutionary change and the origination of new species adapted to new environments. I will discuss a few of these global, regional, and local stresses based primarily on my own research programs. These examples will include the 1) global regional and local experiment of subterranean mammals; 2) regional experiment of fungal life in the Dead Sea; 3) evolution of wild cereals; 4) “Evolution Canyon”; 5) human brain evolution, and 6) global warming.

Predicting the potential distribution of an endangered cryptic subterranean mammal from few occurrence records

Knowledge of geographical distributions and habitat preferences are central to the conservation and management of threatened species. Ecological niche models can be used to map potentially suitable habitat, making them valuable tools in conservation biology. These models can assist in searching for new populations of species with poorly known distributions and can also be used to guide area selection for systematic biodiversity planning. These models have traditionally required ten or more occurrence records for calibration and this has limited the use of these tools in conservation biology, since many threatened species are known from fewer records. However, recently models have been successfully calibrated using few records. To illustrate this, we developed an ecological niche model to map the potential distribution of the endangered Juliana's golden mole ( Neamblysomus julianae) in South Africa so that it could be used in searching for unrecorded populations and for area selection in systematic biodiversity plans. A model was calibrated in Maxent using only four occurrence records. Predictor variables included various bioclimatic, soil and vegetation types. The model identified limited suitable habitat within the map region. The first model facilitated the identification of two previously unrecorded populations. A second model was calibrated using the two additional occurrence records. This increased the proportion of correctly predicted presence records. Jackknife analyses indicated that the models were successful at predicting known presences as suitable. This paper demonstrates the use of ecological niche modelling to conservation of a cryptic endangered species with a poorly known distribution and discusses issues that are relevant for the application of this approach to other species.

A seasonal difference of daily energy expenditure in a free-living subterranean rodent, the silvery mole-rat ( Heliophobius argenteocinereus; Bathyergidae)

In seasonal climatic regimes, animals have to deal with changing environmental conditions. It is reasonable to expect that seasonal changes are reflected in animal overall energetics. The relation between daily energy expenditure (DEE) and seasonally variable ecological determinants has been studied in many free-living small mammals; however with inconsistent results. Subterranean mammals, i.e. fossorial (burrowing) mammals which live and forage underground, live in a seasonally and diurnally thermally stable environment and represent a suitable model to test seasonality in DEE in respect to seasonal changes, particularly those in soil characteristics and access to food supply. Both factors are affected by seasonal rainfall and are supposed to fundamentally determine activity of belowground dwellers. These ecological constraints are pronounced in some tropical regions, where two distinct periods, dry and rainy seasons, regularly alternate. To explore how a tropical mammal responds to an abrupt environmental change, we determined DEE, resting metabolic rate (RMR) and sustained metabolic scope (SusMS) in a solitary subterranean rodent, the silvery mole-rat, at the end of dry season and the onset of rainy season. Whereas RMR did not differ between both periods, mole-rats had 1.4 times higher DEE and SusMS after the first heavy rains. These findings suggest that rainfall is an important environmental factor responsible for higher energy expenditure in mole-rats, probably due to increased burrowing activity. SusMS in the silvery mole-rat is comparable to values in other bathyergids and all bathyergid values rank among the lowest SusMS found in endothermic vertebrates.

Macrophysiology of subterranean mammals. Ctenomys: A model to assess the effect of global warming on physiology and distribution

Macrophysiology of subterranean mammals. Ctenomys: A model to assess the effect of global warming on physiology and distribution

Comparative respiratory strategies of subterranean and fossorial octodontid rodents to cope with hypoxic and hypercapnic atmospheres

Subterranean rodents construct large and complex burrows and spend most of their lives underground, while fossorial species construct simpler burrows and are more active above ground. An important constraint faced by subterranean mammals is the chronic hypoxia and hypercapnia of the burrow atmosphere. The traits, regarded as "adaptations of rodents to hypoxia and hypercapnia", have been evaluated in only a few subterranean species. In addition, well-studied subterranean taxa are very divergent to their sister groups, making it difficult to assess the adaptive path leading to subterranean life. The closely related sister genera Octodon and Spalacopus of Neotropical rodents offer a unique opportunity to trace the evolution of physiological mechanisms. We studied the ventilatory responses of selected octodontid rodents to selective pressures imposed by the subterranean niche under the working hypothesis that life underground, in hypoxic and hypercapnic conditions, promotes convergent physiological changes. To perform this study we used the following species: Spalacopus cyanus (the subterranean coruros) and Octodon degus (the fossorial degus) from central Chile. Ventilatory tidal volume and respiratory frequency were measured in non-anaesthetized spontaneously breathing animals. Acute hypoxic challenges (O(2) 1-15%) and hypercapnia (CO(2) 10%) were induced to study respiratory strategies using non-invasive whole body pletismography techniques. Our results show that coruros have a larger ventilatory response to acute hypoxia as than degus. On the other hand, hypercapnic respiratory responses in coruros seem to be attenuated when compared to those in degus. Our results suggest that coruros and degus have different respiratory strategies to survive in the hypoxic and hypercapnic atmospheres present in their burrows.

Use of resources by the subterranean rodent Ctenomys mendocinus (Rodentia, Ctenomyidae), in the lowland Monte desert, Argentina

The feedback between organisms and their environment is of great relevance to the understanding of ecosystem functioning. Particularly, subterranean mammals living on desert systems play an important role in ecosystem processes modifying their environment and influencing the life strategies of plants and animals. The mendocino tuco-tuco Ctenomys mendocinus, is a fossorial rodent inhabiting a wide range of soil and climate conditions in the central arid lands of Argentina. The purpose of our study was to quantify the degree of environmental segregation: soil properties and vegetation in four habitat types, their impact on woody vegetation, and diet. The highest activity was recorded in sand dunes and was associated with high habitat heterogeneity and soft soils. Degree of herbivory varied among habitats, with Lycium (Solanaceae) being the most gnawed shrub. Tuco-tucos behave like folivorous grazers, feeding on leaves of grasses, mostly Panicum (Poaceae). This is the first study integrating multiple approaches of tucos' auto-ecology in a heterogeneous desert matrix, suggesting a differential use of its environment, possibly according to food supply and soil hardness. Despite life underground impose general constrains for most subterranean species, our results suggest that both above and under ground habitat features play important roles in the occurrence of fossorial rodents.

Burrow architecture and digging activity in the Cape dune mole rat

AbstractWhile females are traditionally thought to invest more time and energy into parental care than males, males often invest more resources into searching and displaying for mates, obtaining mates and in male–male conflict. Solitary subterranean mammals perform these activities in a particularly challenging niche, necessitating energetically expensive burrowing to both search for mates and forage for food. This restriction presumably affects males more than females as the former are thought to dig longer tunnels that cover greater distances to search for females. We excavated burrow systems of male and female Cape dune mole rats Bathyergus suillus the, largest truly subterranean mammal, to investigate whether male burrows differ from those of females in ways that reflect mate searching by males. We consider burrow architecture (length, internal dimensions, fractal dimension of tunnel systems, number of nesting chambers and mole mounds on the surface) in relation to mating strategy. Males excavated significantly longer burrow systems with higher fractal dimensions and larger burrow areas than females. Male burrow systems were also significantly farther from one another than females were from other females' burrow systems. However, no sex differences were evident in tunnel cross‐sectional area, mass of soil excavated per mound, number of mounds produced per unit burrow length or mass of soil excavated per burrow system. Hence, while males may use their habitat differently from females, they do not appear to differ in the dimensions of the tunnels they create. Thus, exploration and use of the habitat differs between the sexes, which may be a consequence of sex differences in mating behaviour and greater demands for food.

African Mole-Rats (Family Bathyergidae): Models for Studies in Animal Physiology

The African mole-rats of the family Bathyergidae are an excellent model group of mammals for undertaking physiological research. The wide spectrum of social organizations, coupled with their underground lifestyles, make this unique family ideal for studies that embrace broad principles in physiology. Here I present an overview of past and ongoing research into the energetics, locomotory activity patterns, pineal melatonin function and reproductive physiology of these fascinating subterranean mammals.

Insights into torpor and behavioural thermoregulation of the endangered Juliana's golden mole

AbstractThe cryptic, subterranean ways of golden moles (Chrysochloridae) hamper studies of their biology in the field. Ten species appear on the IUCN red list, but the dearth of information available for most inhibits effective conservation planning. New techniques are consequently required to further our understanding and facilitate informed conservation management decisions. We studied the endangered Juliana's golden mole Neamblysomus julianae and aimed to evaluate the feasibility of using implantable temperature sensing transmitters to remotely acquire physiological and behavioural data. We also aimed to assess potential body temperature (Tb) fluctuations in relation to ambient soil temperature (Ta) in order to assess the potential use of torpor. Hourly observations revealed that Tb was remarkably changeable, ranging from 27 to 33 °C. In several instances Tb declined during periods of low Ta. Such ‘shallow torpor’ may result in a daily energy saving of c. 20%. Behavioural thermoregulation was used during periods of high Ta by selecting cooler microclimates, while passive heating was used to raise Tb early morning when Ta was increasing. In contrast to anecdotal reports of nocturnal patterns of activity, our results suggest that activity is flexible, being primarily dependent on Ta. These results exemplify how behavioural patterns and microclimatic conditions can be examined in this and other subterranean mammal species, the results of which can be used in the urgently required conservation planning of endangered Chrysochlorid species.

Comparative Energetics of the SubterraneanCtenomysRodents: Breaking Patterns

Subterranean mammals show lower mass-independent basal metabolic rates (BMRs). Several competing hypotheses were suggested to explain how microenvironmental conditions and underground life affect subterranean mammalian energetics. Two of these are the thermal stress and the cost-of-burrowing hypotheses. The thermal stress hypothesis posits that a lower mass-independent BMR reduces overheating in burrows where convective and evaporative heat loss is low, whereas the cost-of-burrowing hypothesis states that a lower mass-independent BMR may compensate for the high energy expenditure of digging. In this article, we assessed the relationship between BMR of Ctenomys and environmental variables through conventional statistics as well as independent contrasts. Moreover, we tested both the thermal stress and the cost-of-burrowing hypotheses at an interspecific level in a very homogeneous genus of subterranean rodents, the South American genus Ctenomys. We compared species from different geographic localities that have contrasting habitat conditions. We measured BMR through open-flow respirometry. After conventional as well as independent contrast analyses, our results support neither the thermal stress nor the cost-of-burrowing hypotheses. We observed that only body mass affects the variability in BMR. Contrasting climatic and soil conditions, habitat productivity, and net primary productivity were not correlated with BMR variability. We suggested that, because BMR and maximum metabolic rates (MMRs) are correlated, low BMRs among Ctenomys species could also be determined by factors that affect MMR rather than BMR.

Blind and naked, but oh so cool: The subterranean world of the naked mole‐rat

Are big ears, tails, and eyes simply anatomical "junk" to subterranean mammals? These animals show remarkable convergent evolution for reducing external ears, tails, and eyes. The naked mole‐rat (NMR, Heterocephalus glaber) displays these features, as well as unusual characteristics even among subterraneans (cold‐blooded and completely furless). Whereas visual and auditory spatial cues are of diminished importance, NMRs are specialized for alternative modalities (primarily via mechanoceptors). We are studying yet other unusual characteristics, which include two structures that may be heading for the anatomical junk pile. First, the NMR is the only mammal with a vomeronasal organ (VNO) that shows no post‐natal growth and sexual suppression is not mediated by urinary signals as in other rodents. Second, the nerve network for processing pain from chemicals (acid and capsaicin) is reduced and lacks neuropeptides that usually signal pain. NMRs are the only mammals that feel no pain from these substances. These features may be a result of this species' unusual combination of lifestyle traits (subterranean + hundreds of individuals + extremely social), resulting in CO2 levels high enough to cause acidosis and chemical pain. Coincidentally, the neuropeptides that are lacking from the pain system also mediate the VNO's vascular pump. NMRs provide unique insights into sensory specialization and evolutionary loss.