Georychus Research Articles

Ecology, longevity and naked mole-rats: confounding effects of sociality?

Ecology, longevity and naked mole-rats: confounding effects of sociality?

Adult neurogenesis and its anatomical context in the hippocampus of three mole-rat species.

African mole-rats (family Bathyergidae) are small to medium sized, long-lived, and strictly subterranean rodents that became valuable animal models as a result of their longevity and diversity in social organization. The formation and integration of new hippocampal neurons in adult mammals (adult hippocampal neurogenesis, AHN) correlates negatively with age and positively with habitat complexity. Here we present quantitative data on AHN in wild-derived mole-rats of 1 year and older, and briefly describe its anatomical context including markers of neuronal function (calbindin and parvalbumin). Solitary Cape mole-rats (Georychus capensis), social highveld mole-rats (Cryptomys hottentotus pretoriae), and eusocial naked mole-rats (Heterocephalus glaber) were assessed. Compared to other rodents, the hippocampal formation in mole-rats is small, but shows a distinct cytoarchitecture in the dentate gyrus and CA1. Distributions of the calcium-binding proteins differ from those seen in rodents; e.g., calbindin in CA3 of naked mole-rats distributes similar to the pattern seen in early primate development, and calbindin staining extends into the stratum lacunosum-moleculare of Cape mole-rats. Proliferating cells and young neurons are found in low numbers in the hippocampus of all three mole-rat species. Resident granule cell numbers are low as well. Proliferating cells expressed as a percentage of resident granule cells are in the range of other rodents, while the percentage of young neurons is lower than that observed in surface dwelling rodents. Between mole-rat species, we observed no difference in the percentage of proliferating cells. The percentages of young neurons are high in social highveld and naked mole-rats, and low in solitary Cape mole-rats. The findings support that proliferation is regulated independently of average life expectancy and habitat. Instead, neuronal differentiation reflects species-specific demands, which appear lower in subterranean rodents.

Effects of Laboratory Housing on Exploratory Behaviour, Novelty Discrimination and Spatial Reference Memory in a Subterranean, Solitary Rodent, the Cape Mole-Rat (Georychus capensis)

A large number of laboratory and field based studies are being carried out on mole-rats, both in our research group and others. Several studies have highlighted the development of adverse behaviours in laboratory animals and have emphasised the importance of enrichment for captive animals. Hence we were interested in evaluating how laboratory housing would affect behavioural performance in mole-rats. We investigated exploratory behaviour, the ability to discriminate between novel and familiar environments and reference memory in the solitary Cape mole-rat ( Georychus capensis ). Our data showed that both wild and captive animals readily explore open spaces and tunnels. Wild animals were however more active than their captive counterparts. In the Y maze two trial discrimination task, wild animals failed to discriminate between novel and familiar environments, while laboratory housed mole-rats showed preferential spatial discrimination in terms of the length of time spent in the novel arm. The performance of the laboratory and wild animals were similar when tested for reference memory in the Y maze, both groups showed a significant improvement compared to the first day, from the 3rd day onwards. Wild animals made more mistakes whereas laboratory animals were slower in completing the task. The difference in performance between wild and laboratory animals in the Y-maze may be as a result of the lower activity of the laboratory animals. Laboratory maintained Cape mole-rats show classic behaviours resulting from a lack of stimulation such as reduced activity and increased aggression. However, they do display an improved novelty discrimination compared to the wild animals. Slower locomotion rate of the laboratory animals may increase the integration time of stimuli, hence result in a more thorough inspection of the surroundings. Unlike the captive animals, wild animals show flexibility in their responses to unpredictable events, which is an important requirement under natural living conditions.

Subterranean Sympatry: An Investigation into Diet Using Stable Isotope Analysis

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

Determinants of Helminth Infection in a Subterranean Rodent, the Cape Dune Mole-Rat (Bathyergus suillus)

The helminth fauna of the largest bathyergid, the Cape mole-rat ( Bathyergus suillus ) was studied throughout an entire calendar year. The species richness encountered was low, with only 3 species of nematodes ( Longistriata bathyergi , Mammalakis macrospiculum, and Trichostrongylus sp.) and 2 species of cestodes ( Taenia sp. and Rodentolepis sp.). At less than 10%, the prevalence for all helminths species was similarly low and may be a result of the solitary lifestyle and the subterranean habitat exploited by this rodent. Clear seasonal patterns were apparent for the most common nematode ( L. bathyergi ), and prevalence and abundance were highest among non-pregnant females compared to males and pregnant females. Dispersal patterns associated with the mating system of the host could explain this pattern. In contrast, the prevalence of the most common cestode ( Taenia sp.) was neither determined by season nor host sex, suggesting that foraging habits may constantly expose B. suillus to this parasite.

Low levels of polymorphism at novel microsatellite loci developed for bathyergid mole-rats from South Africa

Eight microsatellite markers were developed for African mole-rats using the Fast Isolation by AFLP of Sequences Containing repeats (FIASCO) protocol and pyrosequencing. The markers were developed in Bathyergus suillus and applied to a selection of individuals from seven related taxa: Bathyergus janetta, Cryptomys hottentotus hottentotus, C. h. pretoriae, Fukomys damarensis, F. darlingi, F. mechowii and Georychus capensis. The markers displayed low to moderate variation with allele numbers ranging between one and six per species. We propose that larger repeat numbers at di-, tri- and tetranucleotide repeat loci generally yield higher levels of polymorphism.

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)

The comparative anatomy of the abdominal gastrointestinal tract of six species of African mole‐rats (Rodentia, Bathyergidae)

The gastrointestinal tracts (GITs) of six species of African mole-rats (Bathyergidae) were compared. The aim was to provide a comprehensive anatomical comparison between the different species. The relative shape, length, and surface areas were taken into account to determine whether the GITs are phylogenetically constrained or exhibit anatomical adaptations in response to diets. In all six species the stomach was simple and glandular. With the exception of Heterocephalus glaber, the caecum was coiled in a flat spiral, the ascending colon was arranged in a loop of varying lengths, and a mucosal colonic papillary-lined groove was present in the ascending colon in all species. By contrast, the caecum in H. glaber was uncoiled, the ascending colon was not looped, and the groove was not papillated. A caeco-appendix was observed only in Bathyergus suillus and Georychus capensis. Hierarchical multivariate cluster analysis on the presence/absence of nine anatomical structures associated with the GIT of mole-rats revealed that H. glaber was anatomically the least similar of the six species (77.6% similarity) with respect to the nine GIT variables included. All Cryptomys species were the same (100% similarity), and two species B. suillus and G. capensis grouped together and were more similar to the Cryptomys genus (95% similarity) than they were to H. glaber. These findings support previous phylogenetic classifications. The voluminous caeco-colon in B. suillus may be explained by its ingestion of grasses in addition to below-ground storage organs of plants. We conclude that phylogeny and diet affect the GIT anatomy of the African mole rats studied here.

Seasonal variation in gonadal steroids of males and females in the Cape mole-rat (Georychus capensis): the potential for opportunistic breeding

Urinary testosterone concentrations in males and urinary progesterone and oestradiol concentrations in females were measured in the Cape mole-rat (Georychus capensis) and compared for the summer and winter periods. The Cape mole-rat breeds seasonally, with sexual activity and subsequent pregnancy recorded during the winter months in the southern hemisphere. Despite the fact that it has a distinct breeding season, seasonal differences in urinary hormone concentrations of both male and female Cape mole-rats were not statistically significant. This finding supports the notion the Cape mole-rat may have the opportunity to operate as an opportunistic breeder if fortuitous environmental conditions arise, such as unseasonal rainfall, occurring at these normally non-favourable times of the year.

Seasonal Variation in Gonadal Steroids of Males and Females in the Cape Mole-Rat (Georychus capensis): The Potential for Opportunistic Breeding

Urinary testosterone concentrations in males and urinary progesterone and oestradiol concentrations in females were measured in the Cape mole-rat (Georychus capensis) and compared for the summer and winter periods. The Cape mole-rat breeds seasonally, with sexual activity and subsequent pregnancy recorded during the winter months in the southern hemisphere. Despite the fact that it has a distinct breeding season, seasonal differences in urinary hormone concentrations of both male and female Cape mole-rats were not statistically significant. This finding supports the notion the Cape mole-rat may have the opportunity to operate as an opportunistic breeder if fortuitous environmental conditions arise, such as unseasonal rainfall, occurring at these normally non-favourable times of the year.

Spatial learning and memory in African mole-rats: The role of sociality and sex

Spatial learning and memory is an important skill for the survival and fitness and may vary between the sexes depending on differences in space use. This is particularly true for animals that explore the subterranean niche as it is associated with high travelling costs. In subterranean rodents the complexity of burrow systems varies with differing degrees of sociality possibly posing stronger selective pressures regarding spatial abilities on species with more complex burrow structures. This could lead to superior abilities in spatial learning and memory in social compared to solitary subterranean species. We tested this hypothesis in two species of subterranean mole-rats, the eusocial Damaraland ( Fukomys damarensis) and solitary Cape mole-rats ( Georychus capensis) by comparing their ability to locate food in an artificial maze. Measurements of the time taken to the goal chamber, the number of wrong turns taken, and the average velocity at which animals travelled were used to compare performance between animals. We did not find marked sex-specific differences in either study species during the assessment of learning and memory retention. In accordance with our hypothesis significant differences between the species were apparent during both learning and memory trials with the social species exhibiting superior performances. However, in both species memory retention was generally high suggesting that the fossorial lifestyle poses a strong selective pressure on spatial abilities in subterranean mammals.

An immunohistochemical study of the gonadotrophin-releasing hormone 1 system in solitary Cape mole-rats, Georychus capensis, and social Natal mole-rats, Cryptomys hottentotus natalensis

Mole-rat species within the family Bathyergidae exhibit a wide range of reproductive strategies and social systems. Various forms of reproductive suppression are displayed within this family: in the solitary species, breeding is suspended for part of the year and in the social species, reproduction is suppressed in subordinate animals. This study investigated the gonadotrophin-releasing hormone 1 (GnHR-1) systems of breeding and non-breeding solitary Cape mole-rats and social Natal mole-rats for possible inter- and/or intra-species differences. In both species, GnRH-1 cell bodies are predominantly in the medial septum region of the diagonal band or the preoptic area, with relatively few in the mediobasal hypothalamus; a dense concentration of GnRH-1-immunoreactive (ir) processes is present in the region of the organum vasculosum of the lamina terminalis. In Cape mole-rats, GnRH-1-ir processes are particularly dense within the lateral margins of the median eminence, which is enfolded by a large pars tuberalis of the pituitary gland. Natal mole-rats display GnRH-1-ir processes across the breadth of the median eminence, which is abutted by a relatively small pars tuberalis. There are more GnRH-1-ir cell bodies in Natal mole-rats than in Cape mole-rats (∼720 vs. ∼420). No significant differences were found in the number, distribution or size of GnRH-1-ir cell bodies according to season in Cape mole-rats or according to reproductive status or sex in Natal mole-rats. In female and male Natal mole-rats, GnRH-1-immunoreactivity in the median eminence is less dense in the reproductive animals; no such difference was found in Cape mole-rats between the breeding and non-breeding seasons. These immunohistochemical results are discussed in the light of earlier studies which identified no functional neuroendocrine impediments underlying regulated reproduction in either Cape or Natal mole-rats. The cumulative findings suggest that the principal factors determining seasonal or socially induced suppression of reproduction in these species are behavioral rather than neuroendocrine.

LH responses to single doses of exogenous GnRH in the Cape mole rat (Georychus capensis): the pituitary potential for opportunistic breeding

AbstractThe Cape mole rat Georychus capensis is a solitary mole rat that inhabits the winter rainfall region of the Western Cape Province of South Africa. Circulating basal concentrations of luteinizing hormone (LH) were found to be significantly higher in the breeding season in both sexes. During both the breeding and non‐breeding season, administration of exogenous gonadotropin‐releasing hormone (GnRH) increased circulatory LH levels. The magnitude of the LH response to an overdose of exogenous GnRH both in and out of the breeding season in males and females was not significantly different. Typically, seasonally breeding species exhibit a down‐regulation of the pituitary and reproductive functions out of the breeding season. It appears that there is no down‐regulation of GnRH receptors at the level of the pituitary out of the breeding season, because the pituitary responds to an exogenous GnRH challenge equally both in and out of the breeding period. The Cape mole rat exhibits the potential for opportunistic breeding out of the breeding period, provided that environmental factors are favourable. This finding questions whether this mole rat is actually a seasonal breeder or whether reproduction is hindered by the ecological constraint of the lack of opportunities to burrow and find mates at certain times of the year.

Penile morphology of African mole rats (Bathyergidae): structural modification in relation to mode of ovulation and degree of sociality

AbstractThe penile morphology and bacular structure of five species of African mole rat are described in relation to the method of ovulation, degree of sociality and polygynandry. We predicted that, with an increase in sociality, and a concomitant decrease in polygynandry and sperm competition, there would be a decrease in penis ornamentation (spinosity) and baculum size. In solitary species of African mole rat with marked seasonal reproduction and induced ovulation (Bathyergus suillus and Georychus capensis), males have numerous epidermal spines on the penis. Social, seasonally breeding, induced ovulating mole rats Cryptomys hottentotus natalensis possess less elaborate ornamentation in the form of small protrusions that are rounded at the apex. Two aseasonally breeding eusocial species with spontaneous ovulation Cryptomys damarensis and Heterocephalus glaber have ridges on the penis but lack any elaborate ornamentation. Baculae, however, showed a trend to become proportionally smaller in the solitary species. Our prediction that, with an increase in sociality and a move from induced to spontaneous ovulation, the amount and degree of penile ornamentation declines was, therefore, generally supported.

Do solitary, seismic signalling Cape mole‐rats (Georychus capensis) demonstrate spontaneous or induced ovulation?

AbstractThe Cape mole‐rat Georychus capensis is a solitary subterranean rodent that exhibits seasonal reproduction. This study set out to determine whether the female Cape mole‐rat is an induced or spontaneous ovulator. Eleven females were collected from the field just before the breeding season and housed individually. Urine was collected for 5 weeks. Females were subjected to one of three trials: housed separately without a male; allowed only non‐physical contact with unvasectomized males; placed in direct contact with four vasectomized males. Urine was collected for a further 5 weeks and urinary progesterone profiles established. Females housed in direct contact with males exhibited heightened progesterone concentrations and the presence of corpora lutea in their ovaries. The act of coitus seems to be necessary for ovulation to occur in the females even though males were not capable of fertilization.

Fos expression in the suprachiasmatic nucleus in response to light stimulation in a solitary and social species of African mole-rat (family Bathyergidae)

Mole-rats are strictly subterranean rodents that are rarely exposed to environmental light. They are well adapted to their environment and have reduced eyes and a severely regressed visual system. It has been shown, however, that mole-rats do exhibit endogenous circadian rhythms that can be entrained, suggesting an intact and functional circadian system. To determine whether light is the entraining agent in these animals, Fos expression in response to light pulses at different circadian times was investigated to obtain phase response curves. Light is integrated effectively in the suprachiasmatic nucleus of the Cape mole-rat ( Georychus capensis), and Fos expression is gated according to the phase of the circadian clock. The Fos response in the Cape mole-rat was comparable to that of aboveground rodents. In contrast, the highveld mole-rat ( Cryptomys hottentotus pretoriae) was less sensitive to light and did not show a selective Fos response according to the phase of the circadian cycle. Social species appear to be less sensitive to light than their solitary counterparts, which compares well with results from locomotor activity studies.

Face pictures reduce behavioural, autonomic, endocrine and neural indices of stress and fear in sheep.

Faces are highly emotive stimuli and we find smiling or familiar faces both attractive and comforting, even as young babies. Do other species with sophisticated face recognition skills, such as sheep, also respond to the emotional significance of familiar faces? We report that when sheep experience social isolation, the sight of familiar sheep face pictures compared with those of goats or inverted triangles significantly reduces behavioural (activity and protest vocalizations), autonomic (heart rate) and endocrine (cortisol and adrenaline) indices of stress. They also increase mRNA expression of activity-dependent genes (c-fos and zif/268) in brain regions specialized for processing faces (temporal and medial frontal cortices and basolateral amygdala) and for emotional control (orbitofrontal and cingulate cortex), and reduce their expression in regions associated with stress responses (hypothalamic paraventricular nucleus) and fear (central and lateral amygdala). Effects on face recognition, emotional control and fear centres are restricted to the right brain hemisphere. Results provide evidence that face pictures may be useful for relieving stress caused by unavoidable social isolation in sheep, and possibly other animal species, including humans. The finding that sheep, like humans, appear to have a right brain hemisphere involvement in the control of negative emotional experiences also suggests that functional lateralization of brain emotion systems may be a general feature in mammals.

Circadian rhythms of locomotor activity in solitary and social species of African mole-rats (family: Bathyergidae).

Mole-rats are strictly subterranean and hardly, if ever, come into contact with external light. As a result, their classical visual system is severely regressed and the circadian system proportionally expanded. The family Bathyergidae presents a unique opportunity to study the circadian system in the absence of the classical visual system in a range of species. Daily patterns of activity were studied in the laboratory under constant temperature but variable lighting regimes in individually housed animals from 3 species of mole-rat exhibiting markedly different degrees of sociality. All 3 species possessed individuals that exhibited endogenous circadian rhythms under constant darkness that entrained to a light-dark cycle. In the solitary species, Georychus capensis, 9 animals exhibited greater activity during the dark phase of the light cycle, while 2 individuals expressed more activity in the light phase of the light cycle. In the social, Cryptomys hottentotus pretoriae, 5 animals displayed the majority of their activity during the dark phase of the light cycle and the remaining 2 exhibited more activity during the light phase of the light cycle. Finally in the eusocial Cryptomys damarensis, 6 animals displayed more activity during the light phase of the light cycle, and the other 2 animals displayed more activity during the dark phase of the light cycle. Since all three mole-rat species are able to entrain their locomotor activity to an external light source, light must reach the SCN, suggesting a functional circadian clock. In comparison to the solitary species, the 2 social species display a markedly poorer response to light in all aspects. Thus, in parallel with the sociality continuum, there exists a continuum of sensitivity of the circadian clock to light.

Seismic Signal Use by Fossorial Mammals1

Abstract The subterranean environment is not favorable for the use of vision or the audition of airborne sounds as means of long-distance sensory perception. However, seismic vibrations have been shown to propagate at least an order of magnitude better than airborne sound between the burrow systems of the mole-rat Georychus capensis. The use of the seismic channel for communication underground is well documented for other species of bathyergids, as well as the spalacine mole-rat Nannospalax. It has recently been suggested that the golden mole Eremitalpa granti namibensis may also be sensitive to ground vibrations, in this case used in foraging in its desert habitat. In this paper, the use of seismic signals among these and other fossorial mammals is reviewed from theoretical, behavioral and anatomical standpoints. The question of whether auditory or somatosensory means are used to detect vibratory signals is examined. Attempts to explain the distribution of seismic sensitivity and communication mechanisms...

Seismic Signal Use by Fossorial Mammals

The subterranean environment is not favorable for the use of vision or the audition of airborne sounds as means of long-distance sensory perception. However, seismic vibrations have been shown to propagate at least an order of magnitude better than airborne sound between the burrow systems of the mole-rat Georychus capensis. The use of the seismic channel for communication underground is well documented for other species of bathyergids, as well as the spalacine mole-rat Nannospalax. It has recently been suggested that the golden mole Eremitalpa granti namibensis may also be sensitive to ground vibrations, in this case used in foraging in its desert habitat. In this paper, the use of seismic signals among these and other fossorial mammals is reviewed from theoretical, behavioral and anatomical standpoints. The question of whether auditory or somatosensory means are used to detect vibratory signals is examined. Attempts to explain the distribution of seismic sensitivity and communication mechanisms among fossorial mammals are considered. The potential influences of different soil type and digging methods are discussed, and it is proposed that digging mechanisms involving the head might preadapt a fossorial mammal towards the development of seismic sensitivity.