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.     

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.     

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.     

Natural history and burrow system architecture of the silvery mole-rat from Brachystegia woodland

The silvery mole-rat Heliophobius 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, the Brachystegia woodland. 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 of Heliophobius is 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.     

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     

Estimation of N2 fixation based on differences in the natural abundance of 15N among freshwater N2-fixing and non-N2-fixing algae

The hypothesis that small mammal burrows can increase the amount of water infiltrating into the soil profile was tested. The amount of water added to the soil profile from spring recharge in areas adjacent to ground squirrel (Spermophilus townsendii and S. elegans) burrows was compared to nearby areas without burrows. Recharge amounts in burrow areas were significantly higher than nonburrow areas. An average of 21% more of the winter precipitation infiltrated into the soil near burrows. The amount of recharge was also found to be positively related to burrow density. Burrows also affected the distribution of the recharge by adding significantly more water to the deeper portions (>50 cm) of the soil profile.     

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.     

Acoustic communication underground: vocalization characteristics in subterranean social mole-rats (Cryptomys sp., Bathyergidae)

In captive adult Zambian mole-rats 14 different sounds (13 true vocalizations) have been recorded during different behavioural contexts. The sound analysis revealed that all sounds occurred in a low and middle frequency range with main energy below 10 kHz. The majority of calls contained components of 1.6–2 kHz, 0.63–0.8 kHz, and/or 5–6.3 kHz. The vocalization range thus matched well the hearing range as established in other studies. The frequency content of courtship calls in two species of Zambian Cryptomys was compared with that in naked mole-rats (Heterocephalus glaber) and blind mole-rats (Spalax ehrenbergi) as described in the literature. The frequency range of maximum sound energy is negatively correlated with the body weight and coincides with the frequencies of best hearing in the respective species. In general, the vocalization range in subterranean mammals is shifted towards low frequencies which are best propagated in underground burrows. Accepted: 16 September 1996     

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.     

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.     

Habitat and sediment preferences ofAxarus festivus larvae

During fall draw-down of a reservoir in northeast Kansas it was observed that larvae ofAxarus festivus were restricted to highly weathered Pennsylvanian Shale outcrops and surrounding coarse sediments with high-clay content derived from erosion of the shale outcroppings. Larvae constructed burrows into the outcrops and eroded coarse sediments, which they used to filter feed by setting up currents through the burrows. Burrows were widely distributed over the outcrops, with average densities ranging from 372–2,351 burrows m^–2. However, closer inspection revealed that burrows were more common at apices of individual shale strata, where weathering of the outcrop was most advanced. Here burrows were more uniformly distributed and densities ranged to 4,166 burrows m^–2. 73% of burrows contained larvae. Burrows were generally U-shaped, and averaged 1.8 mm in diameter and 42 mm in total length. Laboratory experiments revealed that 4th instar larvae removed from burrows could construct new burrows in weathered shale, but preferentially used old empty burrows if available. When given choices among alternative sediment combinations of sandvs. finely-ground shale, sandvs. coarsely-ground shale, and finely-ground shalevs. coarsely-ground shale, larvae exhibited statistically significant preferences for the finely-ground shales (P<0.001), coarsely-ground shales (P<0.001), and coarsely-ground shales (P<0.01), respectively. It is concluded that larvae (1) actively select shale or high-clay content sediments, (2) can differentiate among sediments with differing physical properties and (3) exhibit behavioral choices for sediment types that guide them toward shale outcrops.     

Burrow Architecture of the Ghost Crab Ocypode ceratophthalma on a Sandy Shore in Hong Kong

The ghost crab Ocypode ceratophthalma (Pallas) creates burrows of variety shapes at different ages. Juveniles (mean carapace length 11 mm) produced shallow J-shaped burrows, which incline vertically into the substratum (mean depth 160 mm). Larger crabs (17–25 mm carapace length) have Y-shaped and spiral burrows (mean depth 361 mm). These Y-shaped burrows have a primary arm, which extends to the surface forming the opening, and a secondary arm which terminates in a blind spherical ending. The two arms join in a single shaft and end with a chamber at the base. The secondary arms and chambers are believed to be used for mating or as a refuge from predation. The spiral burrows have spiral single channel ending in a chamber. Older crabs (mean carapace length 32.6 mm) had simple, straight single tube burrows, which inclined into the substratum at mean of 73° and had a mean depth of 320 mm. During summer daytime periods, the burrows shelter the crabs from heat and desiccation stress. The sand surface temperature at the burrow opening was ~48 °C but temperatures inside the burrows can drop to 32 °C at a depth of 250 mm. Variation in the burrow architecture with crab age appears to be related to the crab’s behaviour. Juvenile crabs have smaller gill areas and move out of the burrows regularly to renew their respiratory water and, as a result, they do not need a deep burrow. Larger crabs, in contrast, can tolerate prolonged periods without renewing their respiratory water and therefore create deeper and more complex burrows for mating and refuges.     

High prevalence of <Emphasis Type="Italic">Yersinia pestis</Emphasis> in black-tailed prairie dog colonies during an apparent enzootic phase of sylvatic plague

Sylvatic plague (Yersinia pestis) was introduced into North America over 100 years ago. The disease causes high mortality and extirpations in black-tailed prairie dogs (Cynomys ludovicianus), which is of conservation concern because prairie dogs provide habitat for the critically endangered black-footed ferret (Mustela nigripes). Our goal was to help elucidate the mechanism Y. pestis uses to persist in prairie ecosystems during enzootic and epizootic phases. We used a nested PCR protocol to assay for plague genomes in fleas collected from prairie dog burrows potentially exposed to plague in 1999 and 2000. No active plague epizootic was apparent in the 55 prairie dog colonies sampled in 2002 and 2003. However, 63% of the colonies contained plague-positive burrows in 2002, and 57% contained plague-positive burrows in 2003. Within plague-positive colonies, 23% of sampled burrows contained plague-positive fleas in 2002, and 26% contained plague-positive fleas in 2003. Of 15 intensively sampled colonies, there was no relationship between change in colony area and percentage of plague-positive burrows over the two years of the study. Some seasonality in plague prevalence was apparent because the highest percentages of plague-positive colonies were recorded in May and June. The surprisingly high prevalence of plague on study area colonies without any obvious epizootic suggested that the pathogen existed in an enzootic state in black-tailed prairie dogs. These findings have important implications for the management of prairie dogs and other species that are purported to be enzootic reservoir species.     

两种代表性蚯蚓对设施菜地土壤微生物群落结构及理化性质的影响

不同生态型蚯蚓的取食偏好和生境有所差异,因此蚯蚓的生态型差异可能关乎其对土壤性质的不同影响;有关不同生态型蚯蚓对土壤性质尤其是微生物学性质影响的研究有助于了解蚯蚓生态功能的作用机制。在野外调控试验的第4年采集土壤,研究了牛粪混施和表施处理下内层种威廉腔环蚓(Metaphire guillelmi)和表层种赤子爱胜蚓(Eisenia foetida)对设施菜地土壤微生物群落结构和主要理化性质的影响。结果表明,土壤微生物群落结构同时受到蚯蚓种类和牛粪施用方式的影响。牛粪表施时,两种蚯蚓均显著降低了菌根真菌、真菌生物量和原生动物生物量(P0.05);牛粪混施时,不同蚯蚓的影响有所差异,威廉腔环蚓明显增加了菌根真菌、真菌生物量和放线菌生物量,而赤子爱胜蚓的作用不明显。此外,两种蚯蚓均提高了土壤孔隙度、团聚体稳定性和土壤p H、矿质氮以及微生物生物量碳氮水平,但提高幅度取决于蚯蚓种类和牛粪施用方式。冗余分析表明蚯蚓影响下土壤微生物群落结构的变化与团聚体稳定性、p H、速效磷、矿质氮呈正相关,而与土壤容重呈负相关。     

Vocal repertoire of the social Mashona mole-rat (Fukomys darlingi) and how it compares with other mole-rats

Vocalizations play a major role in communication of mammals with subterranean lifestyles since other senses are dramatically restricted in the environment of below ground burrows. In our study, we recorded vocalizations of 10 adult males and 10 adult females of a social bathyergid, the Mashona mole-rat (Fukomys darlingi) in different behavioural contexts. Vocalizations were divided into four categories according to behavioural contexts. Similar to other subterranean mammals, the range of Mashona mole-rat calls is shifted towards lower frequencies. We described 10 types of true vocal signals and 2 mechanical sounds. The vocal repertoire of the Mashona mole-rat is less rich compared to other social mole-rats, corresponding with its low mean family size. Interestingly, this species has a higher diversity in contact and distress calls, while using a relatively low number of aggressive signals.     

Passive irrigation and functional morphology of crustacean burrows in a tropical mangrove swamp

Flushing measurements and a resin cast of a burrow inhabited by Sesarma messa and Alpheus cf macklay were taken from a Rhizophoraspp. forest. The burrow had 9 openings and occupied a swamp surface area of 0.64 m². Passive irrigation of the burrow was investigated by recording change in conductivity of burrow water in a chamber 45 cm below the swamp surface during tidal inundation of the swamp. The chamber was completely flushed within approximately one hour, i.e. by a single tidal event. Burrow morphology was determined by means of resin casting. The investigated burrow was of discrete structure, with an overall depth of 1.2 m and a total volume of 68 l, i.e. ca. 9% of the volume of swamp soil. The below ground surface area of chambers and tunnels was 3.8 m². The mean and maximum chamber/tunnel diameter was 7 cm and 11 cm respectively. The soil in the close vicinity of the burrow was extensively penetrated by roots, and any two parts of the burrow were located no further than 20 cm away from each other. By reducing diffusion distances within the soil and by being well flushed, the burrows provide an efficient mechanism for removal of excess salt accumulated in the soil around mangrove roots due to exclusion.     

Blunted neuronal calcium response to hypoxia in naked mole-rat hippocampus

Naked mole-rats are highly social and strictly subterranean rodents that live in large communal colonies in sealed and chronically oxygen-depleted burrows. Brain slices from naked mole-rats show extreme tolerance to hypoxia compared to slices from other mammals, as indicated by maintenance of synaptic transmission under more hypoxic conditions and three fold longer latency to anoxic depolarization. A key factor in determining whether or not the cellular response to hypoxia is reversible or leads to cell death may be the elevation of intracellular calcium concentration. In the present study, we used fluorescent imaging techniques to measure relative intracellular calcium changes in CA1 pyramidal cells of hippocampal slices during hypoxia. We found that calcium accumulation during hypoxia was significantly and substantially attenuated in slices from naked mole-rats compared to slices from laboratory mice. This was the case for both neonatal (postnatal day 6) and older (postnatal day 20) age groups. Furthermore, while both species demonstrated more calcium accumulation at older ages, the older naked mole-rats showed a smaller calcium accumulation response than even the younger mice. A blunted intracellular calcium response to hypoxia may contribute to the extreme hypoxia tolerance of naked mole-rat neurons. The results are discussed in terms of a general hypothesis that a very prolonged or arrested developmental process may allow adult naked mole-rat brain to retain the hypoxia tolerance normally only seen in neonatal mammals.     

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.     

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.