Home-Range Dynamics in a Solitary Subterranean Rodent

Despite an important role of subterranean rodents as ecosystem engineers, their belowground mobility is poorly documented. It is supposed that their underground burrow systems, once established, are relatively stable because of high-energy costs of digging. We chose the silvery mole-rat, Heliophobius argenteocinereus (Bathyergidae, Rodentia) from mesic Afrotropics as a representative of solitary subterranean rodents to investigate how, and how fast these rodents process their established burrow systems. We combined radio-tracking of individual animals with subsequent mapping of their burrow systems, and we developed a new method for assessing the rate of burrowing. Mole-rats continuously rebuilt their burrow systems; they excavated approx. 0.7 m of new tunnels per day and backfilled on average 64% of all tunnels. On average, every 32 d they established a new nest. They often completely backfilled newly excavated peripheral burrows, while other parts of their burrow systems were more permanent. Their home-ranges were dynamic and continuously shifted in space. Burrow system processing continued even in the advanced dry season, when soil is difficult to work.     

Energetics in a solitary subterranean rodent, the silvery mole-rat, Heliophobius argenteocinereus, and allometry of RMR in African mole-rats (Bathyergidae)

Low resting metabolic rate (RMR) in subterranean rodents used to be considered as a physiological adaptation to cope with stresses of the belowground environment. In African mole-rats (Bathyergidae, Rodentia), RMR was reported to be independent of body mass. This deviation from a general mammalian pattern was considered a precondition for evolution of eusociality, occurring in some bathyergids. We measured metabolic rate and thermoregulation in the silvery mole-rat, Heliophobius argenteocinereus, the only bathyergid genus for which well-supported, comparable data were still missing. Low RMR (154.04 mL O(2) h(-1), which is 82% of the value predicted for a rodent) corresponds to the value expected in a subterranean rodent. Broad range of the thermoneutral zone (25-33 degrees C) and only slightly higher conductance (17.3 mL O(2) h(-1) degrees C(-1), i.e. 112.5% of that predicted for subterranean mammals) indicate that H. argenteocinereus is adapted to lower burrow temperatures rather than to high temperatures. Low RMR in this solitary species, as in other subterranean rodents in general, is probably associated particularly with high energetic cost of foraging. Our results combined with data on other mole-rats show clearly that RMR within the Bathyergidae is mass-dependent.     

Resource characteristics and foraging adaptations in the silvery mole-rat (<Emphasis Type="Italic">Heliophobius argenteocinereus</Emphasis>), a solitary Afrotropical bathyergid

The African mole rats (Bathyergidae) is a rodent family unique for subterranean life and diverse social systems. Solitary species are thought to be confined to areas with abundant, evenly distributed food resources and easily workable soils, which favors early natal dispersal and independent reproduction. However, there is a paucity of empirical data confirming this assumption. We examined ecological conditions of a typical natural habitat of the solitary silvery mole-rat (Heliophobius argenteocinereus), which is the Miombo woodland, and we identified behavioral and other adaptations which potentially improve its foraging success. We also tested food selectivity of captive mole-rats. In the Miombo, mole-rat food resources were clumped, but relatively ample. This, along with a predictable and relatively short period of year with dry and difficult-to-work soil, creates relatively moderate ecological conditions. Analysis of food stores showed that food storing alone probably does not secure enough food to overcome the advanced dry season in this species. In light of this, several other adaptations, such as food generalism and area-restricted search can assist silvery mole-rats retaining positive energy balance during these times. Food-preference tests showed that silvery mole-rats prefer tubers with high sugar content, followed by those with high water content.     

Thermal biology of a strictly subterranean mammalian family,the African mole-rats (Bathyergidae,Rodentia) - a review

African mole-rats are subterranean rodents, which rarely if ever leave the safety of their burrow systems. The environment of the burrows is humid, with relatively stable temperatures, and may have a hypoxic and hypercapnic atmosphere. One of crucial problems related to the subterranean way of life in mammals is avoidance of overheating, because traditional mammalian cooling mechanisms are not effective under high humidity. In African mole-rats, a variety of adaptations have evolved in response to this and other challenges of the underground ecotope. Traditionally, attention has been devoted mainly to the naked mole-rat Heterocephalus glaber, which became popular as a result of its eusociality and absence of fur, both being unique phenomena in small mammals. Despite more recent research, information on other species is still relatively limited and patchy. I review the results of studies on African mole-rats that are relevant for the understanding of their energetics and thermal biology. Attention is paid to the parameters of the burrow environment, which represent the main selection pressures shaping their physiology. In addition, an overview is given of the morphological, physiological and behavioural adaptations helping mole-rats to face temperature extremes, mechanisms by which they deal with a surplus of metabolic heat and how changes in ambient temperature influence their daily activity. The naked mole-rat is compared to its furred relatives to determine whether this species is really exceptional from the point of thermal biology. An ordination analysis was conducted using published data on mole-rat body temperature, thermoneutral zone, resting metabolic rate and thermal conductance. Most of the variability in these characteristics was found to be explained by body mass, followed by temperature characteristics of climate, but not precipitation, of the species distributional ranges. This analysis shows that the naked mole-rat is comparable to the other mole-rat species in these physiological characteristics.     

Reactions to disturbances in the context of antipredatory behaviour in a solitary subterranean rodent

We investigated reactions of free-living silvery mole-rats (Heliophobius argenteocinereus) to anthropogenic disturbances. Mole-rats detected soil vibrations caused by man carefully walking at a distance of up to 6 m (proved by radio-telemetry). Occasionally, mole-rats encountered outside a nest retreated there after this type of disturbance. After having their burrows broken into, the mole-rats retreated into deep tunnels, separating themselves from the rest of the burrows by soil plugs. Trapping success of silvery mole-rats using live traps for subterranean rodents was low, which contrasts with data so far published on social bathyergids. Antipredatory function of examined behaviours is discussed.     

Burrow architecture,family composition and habitat characteristics of the largest social African mole-rat: the giant mole-rat constructs really giant burrow systems

Among African mole-rats, the giant mole-rat Fukomys mechowii is the largest social species. Despite several attempts to study a free-living population, information on its biology from natural habitats is very scarce. We mapped two neighbouring burrow systems of the giant mole-rat in a miombo woodland in Zambia. We provide information on the size and kin structure of the respective mole-rat families, architecture of their burrow systems, and characteristics of the food supply and soil around the two mapped and additional ten burrow systems. Both uncovered burrow systems were very large (total lengths, 2,245 and 743 m), making them the largest burrow systems ever mapped. Food resources around the additional ten burrow systems had a clumped distribution (standardized Morisita index of dispersion = 0.526), but a relatively high biomass (298 ± 455 g m⁻²). This, together with favourable soil conditions even in the advanced dry season (cone resistance, 328 ± 50 N m⁻²; soil density, 1.36 ± 0.06 g cm⁻³) indicates relatively hospitable ecological conditions. Both food supply and soil conditions were comparable with the conditions found in a miombo habitat of the solitary silvery mole-rat in Malawi. This suggests that there are no ecological constraints which would preclude the solitary life of a subterranean herbivore from the examined habitat. Microsatellite analysis supported the assumption that giant mole-rats live in monogamous multigenerational families with only one breeding pair of non-related animals and their offspring. The mean family size is consistent with previous findings on this species and comparable to that found in other Fukomys species studied thus far.     

What determines the way of deposition of excavated soil

Subterranean rodents continuously extend their burrow systems primarily in search of food, which has an important impact on the ecosystem in which they live. Excavated soil may be pushed either into aboveground mounds or into tunnels underground. Factors affecting the amount of burrowing and the preference of aboveground or underground soil deposition are, nevertheless, little known. We investigated the influence of food supply, soil hardness, and the animal’s body mass on the mode of soil deposition in ten burrow systems of free ranging silvery mole-rats Heliophobius argenteocinereus Peters, 1846. In each burrow system, we estimated the volume of backfilled tunnels and the volume of soil deposited aboveground. The highest amount of variation in these parameters was explained by the interaction of food supply and soil hardness. The ratio of the volume of backfilled tunnels to the volume of mounds was not significantly dependent on any of the explanatory variables. The proportion of backfilled tunnels decreased with the increasing volume of the complete burrow system. We propose that both low food supply and soft soil lead to an increased amount of burrowing, which results in a larger volume of soil deposited both above ground and under ground over a given period of time.     

Light Perception in Two Strictly Subterranean Rodents: Life in the Dark or Blue?

Background

The African mole-rats (Bathyergidae, Rodentia) are strictly subterranean, congenitally microphthalmic rodents that are hardly ever exposed to environmental light. Because of the lack of an overt behavioural reaction to light, they have long been considered to be blind. However, recent anatomical studies have suggested retention of basic visual capabilities. In this study, we employed behavioural tests to find out if two mole-rat species are able to discriminate between light and dark, if they are able to discriminate colours and, finally, if the presence of light in burrows provokes plugging behaviour, which is assumed to have a primarily anti-predatory function.

Methodology/Principal Finding

We used a binary choice test to show that the silvery mole-rat Heliophobius argenteocinereus and the giant mole-rat Fukomys mechowii exhibit a clear photoavoidance response to full-spectrum (“white”), blue and green-yellow light, but no significant reaction to ultraviolet or red light during nest building. The mole-rats thus retain dark/light discrimination capabilities and a capacity to perceive short to medium-wavelength light in the photopic range of intensities. These findings further suggest that the mole-rat S opsin has its absorption maximum in the violet/blue part of the spectrum. The assay did not yield conclusive evidence regarding colour discrimination. To test the putative role of vision in bathyergid anti-predatory behaviour, we examined the reaction of mole-rats to the incidence of light in an artificial burrow system. The presence of light in the burrow effectively induced plugging of the illuminated tunnel.

Conclusion/Significance

Our findings suggest that the photopic vision is conserved and that low acuity residual vision plays an important role in predator avoidance and tunnel maintenance in the African mole-rats.     

Growth and development in six species of African mole-rats (Rodentia: Bathyergidae)

The bathyergid mole-rats provide a unique example of a family of subterranean rodents exhibiting a broad spectrum of sociality. Three genera comprise solitary, strongly territorial individuals whereas two genera are social. This sociality culminates in the eusocial naked mole-rat, Heterocephalus glaber . The pups of solitary mole-rats disperse, establish and thereafter defend their own burrow systems when approximately two months old, whereas those of social genera join an established natal colony. This paper examines whether these different lifestyles are reflected in the early development and rate of growth of pups of mole-rats.
Although the trends are not clear-cut, it is apparent that the pups of solitary genera grow and mature more rapidly than those from social genera. Thus, the growth rate constant ( K ) for the first70–80 days of postnatal growth (using the Gompertz equation) for the solitary genera was between 0.042 and 0.052 day⁻¹, whereas that of the social mole-rats was considerably lower (0.01 5 day⁻¹). Similarly the mean growth rates of solitary genera ranged between 3.3 and 1.227g/day while those of the social mole-rats were 0.229-0.233 g/day.
The pattern of development and the rates of growth in solitary bathyergids are similar to those of other solitary subterranean rodents. One interesting feature common to all the social genera studied to date was that the first pups recruited to a 'new colony', consisting of a reproductive pair of adult mole-rats, grew at a significantly faster rate than pups born to an established colony.     

Evidence from intron 1 of the nuclear transthyretin (Prealbumin) gene for the phylogeny of African mole-rats (Bathyergidae)

A 900- to 1100-bp fragment encompassing intron 1 of the nuclear transthyretin (prealbumin) gene was examined in 12 taxa of Old World hystricognath rodents of the families Bathyergidae, Petromuridae, Thryonomyidae, and Hystricidae. Within the Bathyergidae, Heterocephalus glaber (naked mole-rat) was basal, and the other East African species, Heliophobius argenteocinereus (silvery mole-rat), was sister to a southern African clade containing Bathyergus, Cryptomys, and Georychus (dune, common, and cape mole-rats). These results are congruent with studies using mitochondrial 12S rRNA gene sequences. A combined analysis of transthyretin and 12S rRNA data resulted in a well-supported topology with better resolution than either gene analyzed separately. These data support the findings by M. W. Allard and R. L. Honeycutt (1992, Mol. Biol. Evol. 9: 27-40) and R. L. Honeycutt (1992, Am. Sci. 80: 43-53) that complex social systems evolved independently at least twice, in the common and naked mole-rats.     

Burrow architecture and digging activity in the Cape dune mole rat

While 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.     

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.     

Social Structure Predicts Genital Morphology in African Mole-Rats

Background

African mole-rats (Bathyergidae, Rodentia) exhibit a wide range of social structures, from solitary to eusocial. We previously found a lack of sex differences in the external genitalia and morphology of the perineal muscles associated with the phallus in the eusocial naked mole-rat. This was quite surprising, as the external genitalia and perineal muscles are sexually dimorphic in all other mammals examined. We hypothesized that the lack of sex differences in naked mole-rats might be related to their unusual social structure.

Methodology/Principal Findings

We compared the genitalia and perineal muscles in three African mole-rat species: the naked mole-rat, the solitary silvery mole-rat, and the Damaraland mole-rat, a species considered to be eusocial, but with less reproductive skew than naked mole-rats. Our findings support a relationship between social structure, mating system, and sexual differentiation. Naked mole-rats lack sex differences in genitalia and perineal morphology, silvery mole-rats exhibit sex differences, and Damaraland mole-rats are intermediate.

Conclusions/Significance

The lack of sex differences in naked mole-rats is not an attribute of all African mole-rats, but appears to have evolved in relation to their unusual social structure and reproductive biology.     

Nucleotide sequence variation in the mitochondrial 12S rRNA gene and the phylogeny of African mole-rats (Rodentia: Bathyergidae).

Mitochondrial DNA (mtDNA) sequence variation was examined in eight taxa of the African rodent family Bathyergidae, as well as in two taxa representative of the Old-World hystricognathid rodent families Petromyidae and Thryonomyidae. A total of 812 bp, constituting domains I-III of the 12S ribosomal rRNA gene, were compared for each taxon. The high levels of intrafamilial mtDNA sequence divergence observed (average 16.8, range 3.5-23.2) support an ancient origin for the five genera, 20-38 Mya. These data do not support the current subfamilial groupings of the Bathyergidae. The eastern African naked mole-rat, Heterocephalus glaber, is the most basal representative of the family, with the silvery mole-rat, Heliophobius, being the next most basal. South African forms [dune, common, and cape mole-rats (Bathyergus, Cryptomys, and Georychus, respectively)] group together. The independent origin of the common mole-rat, relative to the naked mole-rat, suggests that complex social systems evolved in parallel along different bathyergid lineages. The 12S rRNA gene is not evolving at a higher rate within the rodent lineages, relative to that seen for artiodactyls and primates. Bathyergid rodents appear to fall at an extreme end of the spectrum of mammalian variation, with respect to both transition/transversion ratios and divergence, showing much lower transition/transversion ratios than those previously reported for intrafamilial comparisons.     

The reproductive biology of the Cape mole-rat, Georychus capensis (Rodentia, Bathyergidae)

Georychus capensis is a seasonal breeder with the reproductive potential of producing two litters during the summer breeding season (August to December). These solitary mole-rats signal to each other through the soil, by drumming with their hind feet. This drumming is probably important in spacing the burrow systems and in triggering the onset of reproductive behaviour. In a captive male the onset of drumming was accompanied by a rise in urinary testosterone concentrations and the enlargement of testes and accessory reproductive glands. The male appeared to drum with a different frequency to the female. Courtship is initiated by the male and copulation involves brief multiple intromissions. The gestation period is about 44 days and the mean litter size is 5.9 with a maximum of 10 pups. Development of the pups is relatively rapid. Inter-sibling aggression begins to develop at 35 days, eventually resulting in the pups dispersing when about 60 days old. Body mass increases exponentially from birth to day 60 and the asymptote is reached around day 260. These features are compared with those of other solitary subterranean rodents and with those of the social Bathyergidae ( Cryptomys hottentotus, Cryptomys damarensis and Heterocephalus glaber ).     

The magnetic compass orientation of the burrows of the Damara mole-rat Cryptomys damarensis (Bathyergidae)

In response to reports claiming that part of the ability of mole-rats (Bathyergidae) to orientate with respect to the geomagnetic field involves orientation of their burrow systems in a southward direction, we measured the orientation of burrows of the Damara mole-rat, Cryptomys damarensis , in the Kalahari Desert. It was found that burrow orientation was not significantly different from that expected for a random distribution of compass orientations.     

Evolution of African mole-rat sociality: burrow architecture, rainfall and foraging in colonies of the cooperatively breeding Fukomys mechowii

African mole rats (Bathyergidae) offer an excellent system with which to test theories relating to the evolution and maintenance of sociality in mammals. The aridity food distribution hypothesis (AFDH) suggests that, within the bathyergids, sociality has evolved in response to patterns of rainfall, its effects on food distribution, and the subsequent costs and risks of foraging and dispersal. Here, in the first detailed study of burrow architecture in a social mole-rat species, with data from 32 burrows, we show that in the giant mole-rat Fukomys mechowii burrow fractal dimension increases with colony size and is higher during the rainy season than during the dry season. The mass of food in the burrow increases with fractal dimension and is higher during the rainy season than during the dry season. These results link for the first time colony size, burrow architecture, rainfall and foraging success and provide support for two assumptions of the AFDH, namely that (1) in arid conditions burrowing may be severely constrained by the high costs of digging; and (2) the potential risks of failing to locate food may be mitigated by increases in colony size.     

Foraging in the subterranean social highveld mole-rat (Cryptomys hottentotus pretoriae): an investigation into mass-dependent geophyte use and foraging patterns

The foraging behaviour of captive colonies of the highveld mole-rat Cryptomys hottentotus pretoriae was investigated in an artificial soil-filled burrow system provided with four trays (patches) that varied in geophyte density and mass. An initial trial involving empty trays (only soil) revealed that there was no preference for any specific tray. There were no statistically significant preferences for excavating in any of the patches of different geophyte density. No preferences were evident for excavation in patches containing geophytes of different mass classes. Empty patches seemed to be preferred over patches containing geophytes when combinations of geophyte density/mass were investigated. The duration of handling and the rate of consumption of geophytes were recorded for 23 individuals of two mass classes. Handling time of geophytes was not related to mole-rat sex, but was strongly linked to mole-rat mass class. Handling time of geophytes was related to geophyte mass class. Small geophytes were less profitable to consume. These findings are considered in light of optimal foraging theory and the situation in the field. It was concluded that the mole-rats generally followed the qualitative predictions of optimal foraging theory, although falling short of being energy maximizers.     

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)     

Food availability and foraging by wild colonies of Damaraland mole-rats (Cryptomys damarensis): implications for sociality

We investigated some of the ecological determinants of sociality in the Damaraland mole-rat, including the spatial distribution and biomass of resources (geophytes) available to foraging Damaraland mole-rats in partly vegetated sand dunes in the Kalahari and in grasslands near Dordabis, Namibia, and the foraging behaviour and residency characteristics of colonies at Dordabis. In both study areas, the geophytes had a clumped distribution, but the highest coefficients of dispersion and mean biomass occurred in the Kalahari where the principal food was the gemsbok cucumber. However, because the coefficient of digestibility was lower in geophytes from the Kalahari than from Dordabis, and the mole-rats only ate about half of a gemsbok cucumber, there was less energy available to mole-rats in the Kalahari. At Dordabis, large established colonies occur in the areas with the richest resources and remain resident in the same area for many years; within this area they search (blindly) for food during brief periods when the soil, at burrow depth, is moist and easily worked. Initially, long straight burrows are dug and few bulbs are taken; once the soil dries, minor changes are made to the burrow system as the mole-rats exploit the food patches they located immediately after the rain. Our results show that the characteristics of the resources, and the short time interval during which location of new resources is possible, favour group living; however, the constraints imposed by these features affect large and small colonies in different ways. Small colonies are more likely to fail than large ones and some crucial factors in the survival of these newly formed colonies are the richness of the area in which their burrows are located, and the size of the colony work force available to locate the food. Received: 6 May 1997 / Accepted: 21 August 1997