Heliophobius Research Articles

Phylogeography and cryptic diversity of the solitary‐dwelling silvery mole‐rat, genus Heliophobius (family: Bathyergidae)

AbstractAlongside the eusocial naked mole‐rat, Heterocephalus glaber, Heliophobius argenteocinereus represents the second oldest lineage within the African mole‐rat family Bathyergidae, and phylogenetically intermediate between the East African Het. glaber and the South African genera Bathyergus and Georychus. Across its geographic range, Hel.. argenteocinereus is widely distributed on both sides of the East African Rift System (EARS), and is a key taxon for understanding the phylogeographic patterns of divergence of the family as a whole. Phylogenetic analysis of 62 mitochondrial cyt b sequences, representing 48 distinct haplotypes from 26 geographic locations across the range of Heliophobius, consistently and robustly resolved six genetically divergent clades that we recognize as distinct evolutionary species. Early species descriptions of Heliophobius were synonymized into a monotypic taxonomy that recognized only Hel. argentocinereus. These synonyms constitute available names for these rediscovered cryptic lineages, for which combined morphological and genetic evidence for topotypical populations endorses the recognition of six to eight distinct taxa. Bayesian estimates of divergence times using the fossil Proheliophobius as a calibration for the molecular clock suggest that the adaptive radiation of the genus began in the early Miocene, and that cladogenesis, represented in the extant species, reflects a strident signature of tectonic activity that forged the principal graben in the EARS.

Resource characteristics and foraging adaptations in the silvery mole‐rat (Heliophobius argenteocinereus), a solitary Afrotropical bathyergid

AbstractThe 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.

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.

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?

BackgroundThe 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 FindingWe 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/SignificanceOur 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.

Kinship structure and mating system in a solitary subterranean rodent, the silvery mole-rat

The African mole-rats (Bathyergidae, Rodentia) are subterranean rodents that have evolved a wide range of social organisations varying from solitary to eusocial. Due to some unusual features of their breeding and social systems, much attention has been focused on social species, with solitary species being virtually ignored. Here, we present the first genetic study on the mating system of any solitary mole-rats, the silvery mole-rat (Heliophobius argenteocinereus) - a species which is assumed to be monogamous. Microsatellite markers were used to analyse the mating system and the kinship structure in populations in southern Malawi. Isolation by distance between individuals was apparent in two studied populations, but not in the third, probably, as a result of barriers limiting dispersal in the latter population. Polygyny was found to be a mating system in this population, where a strongly female-biased adult sex ratio was present. In this case, large distances between the burrow systems of mating partners exclude the possibility of belowground searching for mates, suggesting that the males might seek females aboveground. Interestingly, among analysed litters from various localities, one multiple-sired litter was found. Therefore, the results suggest that the mating system in potentially monogamous solitary subterranean rodents may be much more variable than expected and can differ among populations.

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.

Social Structure Predicts Genital Morphology in African Mole-Rats

BackgroundAfrican 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 FindingsWe 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/SignificanceThe 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.

Variation in the digging apparatus of the subterranean silvery mole-rat, Heliophobius argenteocinereus (Rodentia, Bathyergidae): the role of ecology and geography

The skull of most subterranean tooth-digging rodents is markedly affected by their digging mode. In the present study, we investigated the cranial variation in a strictly subterranean, highly specialized Afrotropical tooth-digger, Heliophobius argenteocinereus (Bathyergidae, Rodentia), using a geometric morphometric approach and evaluated the effect of different factors on size and shape differences among four populations. No evidence for sexual dimorphism was found in skull size or shape. The cranial shape variation was large and influenced mainly by the type of habitat (miombo woodland versus farmland and grassland) and the latitudinal gradient. The dorsal side of the skull appears to be more plastic and adaptable to local environments, as well as more independent of size, than the ventral side. Only the shortening of the rostrum is presumably an adaptive process independent of size that leads to an increase of efficacy of the tooth-digging apparatus in Heliophobius, whereas the increase in the in-force and the more procumbent incisors both comprise size-related changes caused by ontogenetic allometric growth. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 97, 822–831.

Home‐Range Dynamics in a Solitary Subterranean Rodent

AbstractDespite 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.

VOCALISATIONS OF THE SILVERY MOLE-RAT: COMPARISON OF VOCAL REPERTOIRES IN SUBTERRANEAN RODENTS WITH DIFFERENT SOCIAL SYSTEMS

ABSTRACT We examined vocalisations of a solitary subterranean rodent, the Silvery Mole-rat Heliophobius argenteocinereus (Bathyergidae). Seven true vocalisations and one mechanical vocalisation were identified. The main frequencies of the analysed sounds (0.34–13.17 kHz) match to a great extent the frequency range suitable for transmission in underground burrows. Due to the narrow frequency range of vocalisations, motivation is predominantly expressed by the rate of tonality rather than by frequency changes. The vocal repertoire of the Silvery Mole-rat perfectly matches to Morton's MS rules, i.e. that low-frequency and harsh vocalisations indicate hostility whereas high tonal calls signalise appeasement or fear. In comparison with social species, this solitary bathyergid produces fewer calls. It lacks contact and alarm calls, but has a rich repertoire of mating calls (mating ends with duet vocalization of male and female). Acoustic signals seem to play a major role in lowering natural aggressiveness during the mating period.

Chromosomal phylogeny and evolution of the African mole-rats (Bathyergidae)

The subterranean African mole-rats (Family Bathyergidae) show considerable variation in their diploid numbers, but there is limited understanding of the events that shaped the extant karyotypes. Here we investigate chromosomal evolution in specimens representative of six genera and an outgroup species, the cane rat Thryonomys swinderianus, using flow-sorted painting probes isolated from the naked mole-rat, Heterocephalus glaber (2n = 60). A chromosomal phylogeny based on the cladistic analysis of adjacent syntenies detected by cross-species chromosome painting was not consistent with that obtained using DNA sequences due, in large part, to the conserved nature of the Bathyergus, Georychus and Cryptomys karyotypes. In marked contrast, the Fukomys and Heliophobius species showed extensive chromosome reshuffling, permitting their analysis by a computational approach that has conventionally been employed in comparative genomic studies for retrieving phylogenetic information based on DNA sequence or gene order data. Using the multiple genome rearrangements (MGR) algorithm and chromosomal rearrangement data detected among F. damarensis, F. darlingi, F. mechowi and the sister taxa B. janetta and Heliophobius argenteocinereus, cytogenetic support for the monophyly of Fukomys and a sister association for F. darlingi + F. damarensis was retrieved, mirroring the published sequence-based topology. We show that F. damarensis, a lineage adapted to arid and climatically unpredictable environments in Southern Africa, is characterized by a large number of fissions the fixation of which has probably been favoured by environmental factors and/or its particular eusocial structure.

Natural history and burrow system architecture of the silvery mole‐rat fromBrachystegiawoodland

AbstractThe silvery mole‐ratHeliophobius argenteocinereus(Bathyergidae) is a solitary subterranean rodent, widely distributed throughout eastern and south‐eastern Africa in a variety of habitats. Here, we provide the first data on its biology in a typical natural habitat, theBrachystegiawoodland. The population density of mole‐rats was low (4.6 ha−1) and its distribution across the study site was random. Contrary to subadults and pups, the sex ratio of adult mole‐rats was highly female biased (1:5.75), probably due to the higher mortality of males as a consequence of their mating strategy. Reproduction ofHeliophobiusis seasonal and pups are born at the beginning of the hot dry season. Burrow systems of the silvery mole‐rat were long, highly branched, reticulated and comparable in fractal dimension to systems of social bathyergids. Variability in burrow architecture was related to the body mass of the burrow occupants, soil hardness and food supply when tested together. Burrow systems with a higher fractal dimension had inhabitants that had a greater body mass. Longer systems were less branched. Nests were typically deeper than foraging tunnels and experienced negligible temperature fluctuations. The microenvironmental characteristics of the subterranean niche including temperature, humidity and soil characteristics are provided for purpose of comparison with other mole‐rat species.

Determinants of Daily Activity Patterns in a Free-Living Afrotropical Solitary Subterranean Rodent

The subterranean ecotope, particularly in tropical regions, is almost free of daily fluctuations in environmental factors that may serve as zeitgebers. The question arises as to whether there is circadian periodicity in the activity of its permanent inhabitants and, if so, how it is induced and maintained. We used radiotelemetry to follow the activity of the silvery mole-rat, Heliophobius argenteocinereus (Bathyergidae), in its natural environment in Malawi during the dry season. Silvery mole-rats were found inside their nests during 63% ± 8% SD of radiofixes; the animals were inactive for 72% ± 8% of the within-nest fixes recorded. Activity tended to decrease over the course of the dry season. Although activity was detected at any time of day, most individuals showed a predictable (mostly unimodal, occasionally bimodal) pattern of activity that was associated with slight daily belowground temperature fluctuations (mostly less than 3°C). In the coldest part of the dry season, overall activity rose with daily temperature. At the beginning of the hot and dry season, the period of enhanced daily activity was shifted to earlier (colder) hours. Mole-rats in the field apparently respond to even slight temperature fluctuations and adjusted their activity accordingly. We propose that burrow temperature can work as zeitgeber of circadian activity in this species.

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.

Patterns of surface temperatures in two mole-rats (Bathyergidae) with different social systems as revealed by IR-thermography

Furred subterranean mammals face the problem of dissipating heat to the environment because high humidity and absence of air flow in sealed belowground tunnels constrain heat loss from body by convection and evaporation. In order to detect body areas responsible for heat loss, surface temperatures in two species of African mole-rats were measured at different ambient air temperatures by infrared thermography. Fur characteristics were also evaluated. Thinner pelage of the ventrum, its moderate temperature and large size suggest that ventral side of the body is the main thermal avenue for heat loss in both species. Interspecific differences could be explained by different fur characteristics connected with social thermoregulation. Compared to the social Fukomys mechowii, the solitary Heliophobius argenteocinereus has denser and longer fur on most of its body; its surface temperature was thus lower than in F. mechowii at lowered ambient temperatures. On the other hand, the denser and longer hair cover in H. argenteocinereus impedes heat dissipation at highest ambient temperatures (and probably also during digging activity) resulting in increase of core body temperature. H. argenteocinereus seems to be more sensitive to overheating than F. mechowii. At lower air temperatures, the social species may uses huddling to combat hypothermia.

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.

THREE NEW SPECIES OF EIMERIA (APICOMPLEXA: EIMERIIDAE) FROM THE SILVERY MOLE RAT HELIOPHOBIUS ARGENTEOCINEREUS PETERS, 1846 (RODENTIA: BATHYERGIDAE) FROM MALAWI

Three species of Eimeria Schneider are described from feces of the African bathyergid rodent, Heliophobius argenteocinereus, from Malawi. Oocysts of Eimeria heliophobii n. sp. are broadly ellipsoidal; 27.9 (22-31) x 22.3 (18-24.5) microm with a brownish, heavily pitted oocyst wall, and vacuolar oocyst residuum. Sporocysts are oval, 12.8 (12-14) x 8.4 (8-9) microm with Stieda and substieda bodies. Eimeria nafuko n. sp. has subspherical oocysts; 15.5 (15-16) x 12.8 (12-13) microm with a smooth, colorless oocyst wall. Sporocysts are oval, 9.2 (9-10) x 5.3 (5-6) microm, with a small Stieda body; the substieda body is not visible. Oocysts of Eimeria yamikamiae n. sp. are broadly ellipsoidal to subspherical; 20.8 (19-22) x 17.5 (15.5-19) microm, with slightly yellowish, very faintly pitted oocyst wall. The majority of oocysts contained a single spherical vesicular oocyst residuum and numerous very small granules. Sporocysts are oval, 10.7 (10-11) x 6.8. (6-7) microm, with a dome -like Stieda body and a subspherical to lentil-like substieda body. Typically, infected rodents shed oocysts of more than 1 species of Eimeria.

Emmonsiosis of subterranean rodents (Bathyergidae, Spalacidae) in Africa and Israel

The presence of adiaspores of the fungal genus Emmonsia was examined in the lungs of 85 mole rats representing 3 subterranean genera: blind mole rats (Spalax galili and S. golani) from Israel, Ansell's mole-rats (Cryptomys anselli) from Zambia, and silvery mole-rats (Heliophobius argenteocinereus) from Malawi and Zambia. Emmonsiosis was found in 28% of the blind mole rats, 100% of the Ansell's mole-rats, but in none of the silvery mole-rats. Infection in African mole-rats was caused by Emmonsia parva, and infection in Israeli blind mole rats was caused by E. parva and E. crescens. The study indicates that the perennial burrow system of the Ansell's mole-rat forms an appropriate microhabitat for the saprophytic growth of E. parva in Lusaka region, Zambia. We suggest that factors contributing to the striking difference in prevalence of emmonsiosis between the two African mole-rat genera (Cryptomys, Heliophobius) may be their differing burrow types, burrow longevity, and social lives.

Microclimatic stability in burrows of an Afrotropical solitary bathyergid rodent, the silvery mole‐rat (Heliophobius argenteocinereus)

AbstractMean depth and mean size of burrow system components, burrow‐soil temperatures and actual diurnal temperatures, humidity and oxygen concentration in burrows of silvery mole‐rats Heliophobius argenteocinereus were measured in two mesic areas in Malawi. Mesic tropic climate, together with soil and plant cover contribute to a diurnally and seasonally stable microclimate even in shallow burrows. Daily and seasonal changes of burrow temperatures were lower compared to those in bathyergids from temperate areas where ambient and burrow temperatures undergo larger fluctuations. Silvery mole‐rats in Malawi are thus probably not distressed by these environmental factors.