Mashona Mole-rat Research Articles

Otoacoustic emissions in African mole-rats

African mole-rats display highly derived hearing that is characterized by low sensitivity and a narrow auditory range restricted to low frequencies < 10 kHz. Recently, it has been suggested that two species of these rodents do not exhibit distortion product otoacoustic emissions (DPOAE), which was interpreted as evidence for a lack of cochlear amplification. If true, this would make them unique among mammals. However, both theoretical considerations on the generation of DPOAE as well as previously published experimental evidence challenge this assumption. We measured DPOAE and stimulus-frequency otoacoustic emissions (SFOAE) in three species of African mole-rats (Ansell's mole-rat - Fukomys anselli; Mashona mole-rat - Fukomys darlingi; naked mole-rat - Heterocephalus glaber) and found unexceptional otoacoustic emission values. Measurements were complicated by the remarkably long, narrow and curved external ear canals of these animals, for which we provide a morphological description. Both DPOAE and SFOAE displayed the highest amplitudes near 1 kHz, which corresponds to the region of best hearing in all tested species, as well as to the frequency region of the low-frequency acoustic fovea previously described in Ansell's mole-rat. Thus, the cochlea in African mole-rats shares the ability to generate evoked otoacoustic emission with other mammals.

The biology of an isolated Mashona mole-rat population from southern Malawi, with implications for the diversity and biogeography of the genus Fukomys

The Mashona mole-rat, Fukomys darlingi (Thomas, 1895), is a little studied social African mole-rat (Bathyergidae) from south-astern Africa. Here, we present an integrative study characterizing the genetic diversity of populations assigned to F. darlingi with special focus on animals from Nsanje, southern Malawi. These mole-rats show pronounced differences in body mass and general appearance compared to nominate F. darlingi from Zimbabwe and Mozambique, but their taxonomic status has so far remained unclear. A genetic analysis encompassing all major lineages of the genus Fukomys suggests that this population indeed represents a deeply nested lineage within the F. darlingi clade. The karyotype of the Nsanje mole-rats also corresponds to that of the nominate form, being 2n = 54. While both nuclear and mitochondrial data agree about the assignment of the Nsanje mole-rats to F. darlingi, our analyses revealed substantial mitonuclear discordance for other branches within the Fukomys phylogenetic tree. Nsanje mole-rats are significantly larger than nominate F. darlingi and their ontogeny and reproduction closely resemble similar-sized congeneric species rather than the nominate population. The somatic growth of the Nsanje form is the slowest of all African mole-rats. The maximum life span of F. darlingi is at least 19 years. The observed differences between nominate F. darlingi and mole-rats from Nsanje may be attributed mainly to their different body mass. Our study highlights the advantages of an integrative approach for understanding the diversity of African mole-rats and emphasizes the great intraspecific variability that may be encountered in these underground-dwelling rodents.

Unexplored aspects of African mole-rat thermal biology: Daily energy expenditure and development of thermoregulation in Fukomys darlingi (Rodentia: Bathyergidae)

In our study, we analyzed two poorly known aspects of thermal biology in subterranean rodents, the African mole-rats, that being daily energy expenditure and development of thermoregulation in juvenile mole-rat using the social Mashona mole-rat, Fukomys darlingi from southern Malawi. We performed laboratory measurements over 24 h to assess the daily energy expenditure (DEE) in adults as well as the development of the thermoregulatory abilities of juveniles at different ages. To assess the effect of ambient temperature (Ta), we exposed mole-rats to either 30 °C or 20 °C, which represents a thermoneutral as well as a thermally challenging temperature, respectively. The DEE at a Ta of 20 °C was lower than expected based on the calculation from the resting metabolic rate (RMR) at the same Ta, this suggested that heat derived from physical activity can substitute the thermoregulatory heat and thus decrease the cost on thermoregulation. To assess the development of thermoregulation in juveniles and the effect of the presence of family members on it, we measured core body temperature (Tb) and resting metabolic rate (RMR) in juveniles under several social contexts: while alone, with littermates, with littermates and mother and with littermates and both parents. Only juveniles older than one month could generate heat to keep Tb higher than Ta. Thermoregulation appeared to be fully developed in three-month-old juveniles. The presence of adult(s), but not littermates, helped to increase Tb and to decrease the RMR of juveniles. Although the results are mostly preliminary and some interpretations are limited due to low sample size in some social contexts, we may conclude that in this mole-rat species, development of thermoregulation is slow even compared to other altricial mammals.

Analysis of ageing and longevity in African mole-rats – digging deeper than before (Rodentia: Bathyergidae)

African mole-rats (Bathyergidae) have intrigued gerontologists since extreme longevity and intraspecific divergence in ageing rates were demonstrated in some of their representatives. Although many ageing-related papers on African mole-rat species have been published in the last 20 years, a comprehensive overview of lifespan distributions, longevity metrics, and annual mortality rates in different mole-rat species (including solitary ones) is still lacking. In this paper, we aim to fill this gap by (re)analyzing published and hitherto unpublished longitudinal data of five African mole-rat species with different social organizations. We present strong indications that solitary mole-rats age faster than social species, and that the poorly studied Mashona mole-rat Fukomys darlingi exhibits some ageing characteristics not previously reported in other social mole-rats. Our study also provides the first overview of shape metrics of longevity for African mole-rat species intended to serve as a starting point for future updates.

Time tweaks rodents’ subterranean hearing

Scampering through the tunnels of an underground rail station, we might feel like scurrying subterranean rodents, but our well-lit and ventilated tunnels bear little resemblance to the complex communal burrows constructed by rodent excavators. Apart from the lack of oxygen in remote burrow corners, sound carries differently through burrow tunnels than in open air. ‘Frequencies higher than 1 kHz are notably attenuated, even over distances of just a few meters, while lower frequencies are amplified’, says Kai Caspar from the University of Duisburg-Essen, Germany. In addition, the hearing of the rodent species that have descended beneath the surface has altered over time; the question was, had burrowing rodents lost hearing simply through lack of use, or had they actively adapted their hearing to their unique acoustic environment? For example, subterranean rodents could have reduced the sensitivity of their hearing to protect their ears from sounds amplified by tunnels, instead of allowing the sense simply to waste away.To find out, Caspar and his colleagues Alexandra Heinrich, Lea Mellinghaus, Patricia Gerhardt and Sabine Begall (also from the University of Duisburg-Essen) decided to test the hearing of three subterranean species: naked mole rats (Heterocephalus glaber) and Mashona mole rats (Fukomys darlingi), which took to burrowing ∼25 million years ago, and the South American coruro (Spalacopus cyanus), which only adopted a subterranean lifestyle 3.5 million years ago. The team gently anaesthetised the animals, ranging from youngsters to elderly seniors, playing sounds to the slumbering creatures ranging from a low-pitched 30 Hz buzz up to ultrasonic 36 kHz squeals at volumes of 10–80 dB, recording their brainwaves to determine their hearing thresholds at each pitch.And when the researchers compared the rodents’ hearing, it was clear that the hearing of the recent coruro burrowers was far more sensitive than the hearing of the long-term mole-rat excavators. The coruros could still hear ultrasonic sounds up to ∼32 kHz, while the Mashona mole-rats’ hearing tapered out around 4 kHz and the naked mole-rats could barely hear above 6 kHz. Both mole-rat species had lost hearing over the 25 million years since their subterranean shift. Yet, the hearing of all three species was most sensitive to sounds pitched around 1 kHz, which carry most strongly through underground passages. And, when the team recorded conversations between pairs of coruros, Mashona mole-rat duos and a trio of chirping naked mole-rats, the coruros spoke most softly (∼52.6 dB), while the naked mole-rats had the loudest voices ∼58.3 dB, probably to compensate for their poor hearing.So, it seems that rodents don't necessarily lose hearing sensitivity rapidly when they switch to burrowing for a living; coruros haven't done away with their ultrasonic hearing, even though high pitched squeaks barely carry beneath the ground. However, Caspar says, ‘life underground appears to quickly promote a shift of the region of best hearing to low frequencies around 1 kHz’. And, although some aspects of the rodents’ hearing could have dwindled through lack of use, the rodents seem to have tuned their hearing to be most sensitive to a specific range, ‘[possibly] to make the most of the unusual acoustic features of their subterranean homes’, says Caspar.Either way, mole-rat hearing is better than some had thought, in keeping with the creatures’ sociable lifestyle nattering in nest chambers, despite the toll taken over time by their subterranean existence on their appreciation of the squeakier end of the rodent range.

Evoked auditory potentials from African mole-rats and coruros reveal disparity in subterranean rodent hearing.

Hearing in subterranean rodents exhibits numerous peculiarities, including low sensitivity and restriction to a narrow range of comparatively low frequencies. Past studies provided two conflicting hypotheses explaining how these derived traits evolved: structural degeneration and adaptive specialization. To further elucidate this issue, we recorded auditory brainstem responses from three species of social subterranean rodents that differ in the degree of specialization to the underground habitat: the naked mole-rat (Heterocephalus glaber) and the Mashona mole-rat (Fukomys darlingi), which represent the ancient lineage of African mole-rats (Bathyergidae), and the coruro (Spalacopus cyanus), a South American rodent (Octodontidae) that adopted a subterranean lifestyle in more recent geological time. Additionally, we measured call amplitudes of social vocalizations to study auditory vocal coupling. We found elevated auditory thresholds and severe hearing range restrictions in the African mole-rats, with hearing in naked mole-rats tending to be more sensitive than in Mashona mole-rats, in which hearing notably deteriorated with increasing age. In contrast, hearing in coruros was similar to that of epigeic rodents, with its range extending into ultrasonic frequencies. However, as in the mole-rats, the coruros' region of best hearing was located at low frequencies close to 1 kHz. We argue that the auditory sensitivity of African mole-rats, although remarkably poor, has been underestimated by recent studies, whereas data on coruros conform to previous results. Considering the available evidence, we propose to be open to both degenerative and adaptive interpretations of hearing physiology in subterranean mammals, as each may provide convincing explanations for specific auditory traits observed.

Social thermoregulation and socio-physiological effect in the subterranean Mashona mole-rat (Fukomys darlingi)

A strict underground style of life is one of the greatest challenges for mammals partly due to the high energetic cost of obtaining food by digging through a mechanically resistant substrate. Any energy saving adaptation, for example the effect of social thermoregulation, is thus very important for subterranean mammals. It has also been suggested that social mammals may suffer from “isolation stress” if measured alone, because the presence of other family member(s) may decrease the stress levels and thus their metabolic rates. This phenomenon known as a socio-physiological effect should be conspicuous when the metabolism of huddling individuals is measured within a species΄ thermoneutral zone (TNZ), where no energetic costs for body warming or cooling exist. In our study, we measured the resting metabolic rates of a social species of African mole-rat, the Mashona mole-rat (Fukomys darlingi), in individuals, pairs and groups of three to eight individuals. Measurements were carried out at ambient temperature below the species’ TNZ (20 °C) to test the effect of social thermoregulation and at a temperature within the species’ TNZ (30 °C) to test the socio-physiological effect. In pairs, the Mashona mole-rat saved 25% of its individual energetic expenses at the temperature below the TNZ. With increasing group size, energetic savings rose up to four animals, but no savings were found in larger groups. At the temperature within the TNZ, mole-rats saved 10% of individual energetic expenses in pairs, but the difference was not significant. Also, no energetic savings were found in larger groups within the TNZ. Our results on thermoregulatory savings in the TNZ are in contrast with extremely high energetic savings found by other authors in different mole-rat species.

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.

Specific paucity of unmyelinated C‐fibers in cutaneous peripheral nerves of the African naked‐mole rat: Comparative analysis using six species of bathyergidae

In mammalian peripheral nerves, unmyelinated C-fibers usually outnumber myelinated A-fibers. By using transmission electron microscopy, we recently showed that the saphenous nerve of the naked mole-rat (Heterocephalus glaber) has a C-fiber deficit manifested as a substantially lower C:A-fiber ratio compared with other mammals. Here we determined the uniqueness of this C-fiber deficit by performing a quantitative anatomical analysis of several peripheral nerves in five further members of the Bathyergidae mole-rat family: silvery (Heliophobius argenteocinereus), giant (Fukomys mechowii), Damaraland (Fukomys damarensis), Mashona (Fukomys darlingi), and Natal (Cryptomys hottentotus natalensis) mole-rats. In the largely cutaneous saphenous and sural nerves, the naked mole-rat had the lowest C:A-fiber ratio (∼1.5:1 compared with ∼3:1), whereas, in nerves innervating both skin and muscle (common peroneal and tibial) or just muscle (lateral/medial gastrocnemius), this pattern was mostly absent. We asked whether lack of hair follicles alone accounts for the C-fiber paucity by using as a model a mouse that loses virtually all its hair as a consequence of conditional deletion of the β-catenin gene in the skin. These β-catenin loss-of function mice (β-cat LOF mice) displayed only a mild decrease in C:A-fiber ratio compared with wild-type mice (4.42 compared with 3.81). We suggest that the selective cutaneous C-fiber deficit in the cutaneous nerves of naked mole-rats is unlikely to be due primarily to lack of skin hair follicles. Possible mechanisms contributing to this unique peripheral nerve anatomy are discussed. J. Comp. Neurol. 520:2785–2803, 2012. © 2012 Wiley Periodicals, Inc.

Poikilothermic traits in Mashona mole-rat (Fukomys darlingi). Reality or myth?

Abstract [Display omitted] Highlights► We measured metabolic rate of Mashona mole-rat (Fukomys darlingi, Bathyergidae). ► Body temperature (33°C) of F. darlingi was stable even at low ambient temperatures. ► Previously reported poikilothermic traits of F. darlingi were not confirmed. ► Thermoneutral zone of F. darlingi was determined to be from 27 to 34°C. ► Resting metabolic rate of F. darlingi is 0.76mlO2g−1h−1 within thermoneutral zone.

Heterothermy in two mole‐rat species subjected to interacting thermoregulatory challenges

Maintaining a high and constant body temperature (T(b) ) is often viewed as a fundamental benefit of endothermy, but variation in T(b) is likely the norm rather than an exception among endotherms. Thus, attempts to elucidate which factors cause T(b) of endotherms to deviate away from the T(b) that maximizes performance are becoming more common. One approach relies on an adaptive framework of thermoregulation, used for a long time to predict variation in T(b) of ectotherms, as a starting point to make predictions about the factors that should lead to thermoregulatory variation in endotherms. Here we test the predictions that when confronted with thermoregulatory challenges endotherms should (1) become more heterothermic, (2) lower their T(b) setpoint, and/or (3) increase behavioral thermoregulation (e.g., activity levels or social thermoregulation). We exposed two species of relatively homeothermic mole-rats to two such challenges: (a) ambient temperatures (T(a)) well below the thermoneutral zone and (b) increased heat loss caused by the removal of dorsal fur. In general, our results support the adaptive framework of endothermic thermoregulation with each species conforming to some of the predictions. For example, Mashona mole-rats (Fukomys darlingi) increased heterothermy as T(a) decreased, highveld mole-rats (Cryptomys hottentotus pretoriae) displayed lower T(b) 's after shaving, and both species increased behavioral thermoregulation as T(a) decreased. This suggests that there is some merit in extending the adaptive framework to endotherms. However, none of the three predictions we tested was supported under all experimental conditions, reiterating that attempts to determine universal factors causing variation in T(b) of endotherms may prove challenging.

Circadian rhythms of locomotor activity in the subterranean Mashona mole rat, Cryptomys darlingi

The Mashona mole rat, Cryptomys darlingi, is a social, subterranean African rodent that is rarely, if ever, exposed to light, and that exhibits a regressed visual system. This study investigated locomotor activity patterns of Mashona mole rats ( n=12) under different light cycles. Activity was measured using either infrared captors ( n=8) or running wheels ( n=4). The mole rats entrained their activity to a standard (LD 12:12) photoperiod. They displayed either a nocturnal or diurnal activity preference with one bout of activity and one bout of rest. Therefore, as a species, the Mashona mole rat did not show a clear nocturnal or diurnal activity preference. When the LD (12:12) light cycle was inversed, the animals switched their activity, too. Under constant dark (DD), most mole rats (73%) showed a free-running circadian activity rhythm, but under constant light (LL), only some (36%) did. The free-run period of the rhythm ( τ) ranged from 23.83 to 24.10 h. The remaining animals were arrhythmic. There was large interindividual and intraindividual variations in the rate and extent of entrainment, time of activity preference, and activity patterns. Possible reasons for the observed variations are discussed. It is concluded that the Mashona mole rat has an endogenous activity rhythm which approximates 24 h, that the mole rat can distinguish between light and dark, and that the endogenous clock utilises this photic information as a zeitgeber.

Melatonin secretion in the Mashona mole-rat, Cryptomys darlingi—influence of light on rhythmicity

The hormone melatonin is synthesised and secreted from the pineal gland in darkness and triggers the daily and seasonal timing of various physiological and behavioural processes. The Mashona mole-rat, Cryptomys darlingi, lives in subterranean burrows that are completely sealed and is therefore rarely, if ever, exposed to light under natural conditions. Hence, this species is of particular interest for studies on rhythms of melatonin secretion. We investigated how plasma melatonin concentrations of the Mashona mole-rat responded to exposure to a long-term standard photoperiod of 12 h light, 12 h dark (12:12 LD), constant light (LL) and constant dark (DD). In addition, we examined whether plasma melatonin concentration was coupled to locomotor activity. Mashona mole-rats displayed rhythms of plasma melatonin concentration that appeared entrained to the standard LD photoperiod, suggesting that the mole-rat is capable of perceiving and entraining to this photic zeitgeber. Furthermore, under chronic constant lighting conditions (DD, LL), circadian rhythms in plasma melatonin concentration were observed, suggesting the possible existence of an endogenous rhythm. Light suppressed melatonin secretion, but constant light did not abolish the rhythm of plasma melatonin concentration. Between active and non-active animals, no difference in plasma melatonin concentration was found for any of the sequential photoperiods (LD1 DD, LD2, LL), tentatively suggesting that the rhythm of melatonin secretion is uncoupled from that of locomotor activity.

Recrudescence of sexual activity in a colony of the Mashona mole‐rat (Cryptomys darlingi): an apparent case of incest avoidance

AbstractColonies of the Mashona mole‐rat Cryptomys darlingi are founded from a single reproductive pair of animals that are genetically unrelated by descent. All non‐reproductive animals are the progeny of the reproductive pair. Non‐reproductive colony members do not seem to be suppressed from reproduction at the level of the pituitary. In colonies in which the reproductive female is removed or dies, there is strict incest avoidance and the colony remains reproductively quiescent. Reinstatement of sexual activity in a queenless colony may be brought about in the laboratory by the introduction of unfamiliar and unrelated adult males. In the queenless colony under study, there was a marked change in the dominance hierarchy with an increase in Landau's index of linearity from 0.61 to 1.0 on the introduction of two unrelated males. The two new males became the most dominant within the colony. All previously non‐reproductive females exhibited heightened urinary oestradiol 17β and progesterone concentrations on the introduction of the males. However, it was only the older and most dominant non‐reproductive female that became the new reproductive female and produced a litter of three pups 70 days after the initial introduction.

Causes and consequences of incest avoidance in the cooperatively breeding mole‐rat, Cryptomys darlingi (Bathyergidae)

A number of social mole‐rat species maintain a strong reproductive skew (only one breeding pair in the group) solely through incest avoidance. Incest avoidance probably evolved for one of two reasons, namely for actually maintaining a reproductive skew or, alternatively, to avoid high inbreeding depression. In the latter case a strong reproductive skew would result as a fortuitous by‐product of the combination of a cloistral family life style of mole‐rats and incest avoidance. We undertook breeding experiments in which the fertility of pairs of unrelated individuals were compared with that of pairs of double first cousins. Inbreeding depression was remarkably high and an accompanying model suggests that it may be sufficient to support the idea that strong incest avoidance evolved primarily to eliminate the costs of inbreeding and subsequently facilitated the evolution of reproductive skew.

LH responses to single doses of exogenous GnRH by social Mashona mole-rats: a continuum of socially induced infertility in the family Bathyergidae.

The Mashona mole-rat, Cryptomys darlingi, exhibits an extreme reproductive division of labour. Reproduction in the colony is restricted to a single breeding pair. The non-reproductive male and female colony members are restrained from sexual activity by being familiar and related to one another and the reproductive animals. Circulating basal concentrations of luteinizing hormone (LH) as well as LH levels measured in response to a single exogenous gonadotropin releasing hormone (GnRH) challenge are not significantly different between the reproductive and non-reproductive groups of either sex. Socially induced infertility in both non-reproductive males and females does not result from a reduced pituitary secretion of LH or decreased sensitivity to hypothalamic GnRH, but rather appears to result from an inhibition of reproductive behaviour in these obligate outbreeders. The African mole-rats exhibit a continuum of socially induced infertility with differing social species inhabiting regions of varying degrees of aridity. In this continuum a transition from a predominantly behavioural repression in a social mesic-adapted species through to complete physiological suppression lacking incest avoidance in an arid-adapted eusocial species occurs in this endemic African family of rodents.

The social structure and dominance hierarchy of the Mashona mole‐rat, Cryptomys darlingi (Rodentia: Bathyergidae) from Zimbabwe

Cryptomys darlingi is a social subterranean rodent mole which inhabits the mesic regions of south‐eastern and central Africa. Mashona mole‐rats live in small colonies (5‐9 animals) in which reproduction is normally restricted to the largest male and female in the colony. The non‐reproductive members in a mature colony cannot be placed into clearly defined work‐related groups based on body mass.The dominance hierarchy of a young colony was found to be linear, with a value of 1.00 calculated from Landau's linearity index, while that of a mature colony of nine mole‐rats was almost linear (0.77). Dominance was found to be related to gender in the mature colony, with males more dominant than females, and to age in the young colony. The reproductive mole‐rats are the dominant animals within their respective genders. Dominance appears to correlate positively with body mass (rs = 0.77 in the mature colony and rs = 0.93 in the young colony).Popularity studies show that smaller animals and females tend to be more popular than the larger massed individuals or males. In the mature colony which contained predominantly adult animals, the reproductive pair was among the least popular. While in the young colony, composed predominantly of sub‐adult and juvenile animals, the reproductive pair was the most popular.Social organization within Mashona mole‐rat colonies is compared with other southern African Cryptomys species.

Reproductive Sharing in Different Types of Kin Associations

Reproductive Sharing in Different Types of Kin Associations

The colony structure and reproductive biology of the afrotropical Mashona mole‐rat, Cryptomys darlingi

Cryptomys darlingi occurs in the mesic Miombo woodland of north‐eastem Zimbabwe. It occurs in colonies of up to nine individuals, in which reproduction is limited to one of the largest males and the largest female in the colony.Reproduction and details of colony size and number of breeding animals in a colony are described for five complete field‐captured colonies.In captivity, mating is not confined to a particular season, and up to three litters of pups are orn per annum. The reproductive female initiates the pre‐copulatory behaviour. The gestation lengti is 56–61 days (n = 2). The new‐born pups are altricial and litter size is small x̄ = 1.7 ± 0.5 (n = 6). In this case, the pups first left the nest 10 days after birth, began to eat solids when 14 days old, and were fully weaned at five weeks. They began to spar with each other when 36–40 days old, but did not disperse and were incorporated into the colony. This suggests that the Mashona mole‐rat colonies are composed of a founding pair and at least three successive litters of pups.