Wild mice in an urbanized world: Effects of light at night under natural and laboratory conditions in the single-striped grass mouse (Lemniscomys rosalia).

Urbanization, and the accompanying artificial light at night (ALAN), can disrupt the activity of animals. Such disruptions at the base of a food web can ripple through the ecosystem. Most studies of ALAN are performed in the laboratory. Thus, we lack basic information about the circadian responses of animals under natural environmental conditions to fully evaluate the impact of ALAN. We studied the behaviour and activity of wild-caught, peri-urban single-striped grass mice (Lemniscomys rosalia) under a natural treatment and in a standard laboratory treatment, including dim light at night to mimic conditions that they could experience. The species exhibited predominantly crepuscular activity under all experimental treatments. It showed the highest level of activity under the natural treatment, whereas ALAN significantly suppressed its activity. Males were more active than females under all experimental treatments. The marked changes in activity under ALAN is of particular concern since global change in combination with urbanization can lead to a change in vegetation density and composition that will decrease the number of suitable microhabitats and expose small mammals to novel habitat changes. We suggest that the single-striped mice could become vulnerable because of urbanization, leading to impacts on its ecosystem broadly.

Laterality in the Damaraland Mole-Rat: Insights from a Eusocial Mammal.

Lateralization is the functional control of certain behaviors in the brain being processed by either the left or right hemisphere. Behavioral asymmetries can occur at an individual and population level, although population-level lateralization is less common amongst solitary species, whereas social species can benefit more from aligning and coordinating their activities. We assessed laterality (individual and population) through turning biases in the eusocial Damaraland mole rat, Fukomys damarensis. We considered factors such as breeding status (queen or subordinate), environment (wild-caught or captive), sex (male or female), colony and body mass. All individuals together demonstrated significant left-turning biases, which was also significant at the population level. Wild-caught animals were more strongly lateralized, had a wider spread over a laterality index and lacked the population-level left-turning bias as compared to captive mole rats. Subordinate animals were more lateralized than queens, demonstrating social status differences in turning biases for social mole rats. This emphasizes the importance of animal handling and context when measuring and interpreting behavioral asymmetries.

Grazing during the grassland greenup period promotes plant species richness in alpine grassland in winter pastures.

Although grazing is the most common use of grassland, the ecological function of grassland far exceeds its productivity. Therefore, the protection of plant diversity is of the utmost importance and cannot be ignored. Existing research on the effect of grazing on grassland mainly focuses on grazing intensity and the type of livestock, but the consequences of the timing of the grazing on the vegetation community remains unclear. We investigated plant community characteristics of winter pastures in alpine meadow with different grazing termination times (grazing before and during the grassland greenup periods) in Maqu County, eastern QTP. The results showed that vegetation height, coverage, aboveground biomass and Graminoid biomass were lower in grassland when grazing happened during the greenup period compared to grassland where grazing was terminated before the greenup period. However, the total plant species richness and forbs richness were higher in grassland with grazing during the greenup period compared to grassland without grazing during the greenup period. Our structural equation modeling reveals a potential indirect implication for the total plant species richness and forbs richness of winter pastures mainly through a decrease in the vegetation coverage and grass biomass abundance. Our findings imply that grazing during the grassland greenup period may facilitate the maintenance of plant diversity in winter pastures. These findings have important implications for grassland ecosystem functioning and for the conservation of plant diversity.

Physiological rhythms are influenced by photophase wavelength in a nocturnal and a diurnal rodent species from South Africa.

The quality and quantity of light changes significantly over the course of the day. The effect of light intensity on physiological and behavioural responses of animals has been well documented, particularly during the scotophase, but the effect of the wavelength of light, particularly during the photophase, less so. We assessed the daily responses in urine production, urinary 6-sulfatoxymelatonin (6-SMT) and glucocorticoid metabolite (uGCM) concentrations in the nocturnal Namaqua rock mouse (Micaelamys namaquensis) and diurnal four striped field mouse (Rhabdomys pumilio) under varying wavelengths of near monochromatic photophase (daytime) lighting. Animals were exposed to a short-wavelength light cycle (SWLC; ∼465-470 nm), a medium-wavelength light cycle (MWLC; ∼515-520 nm) and a long-wavelength light cycle (LWLC; ∼625-630 nm). The SWLC significantly attenuated mean daily urine production rates and the mean daily levels of urinary 6-SMT and of uGCM were inversely correlated with wavelength in both species. The presence of the SWLC greatly augmented overall daily 6-SMT levels, and simultaneously led to the highest uGCM concentrations in both species. In M. namaquensis, the urine production rate and urinary 6-SMT concentrations were significantly higher during the scotophase compared to the photophase under the SWLC and MWLC, whereas the uGCM concentrations were significantly higher during the scotophase under all WLCs. In R. pumilio, the urine production rate and uGCM were significantly higher during the scotophase of the SWLC, not the MWLC and LWLC. Our results illustrate that wavelength in the photophase plays a central role in the entrainment of rhythms in diurnal and nocturnal African rodent species.

Ambient Temperature as a Strong Zeitgeber of Circadian Rhythms in Response to Temperature Sensitivity and Poor Heat Dissipation Abilities in Subterranean African Mole-Rats.

Mammals have evolved circadian rhythms in internal biological processes and behaviors, such as locomotor activity (LA), to synchronize to the environmental conditions they experience. Photic entrainment of LA has been well established; however, non-photic entrainment, such as ambient temperature (Ta), has received much less attention. To address this dearth of knowledge, we exposed two subterranean endothermic-homeothermic African mole-rat species, the solitary Cape mole-rat (Georychus capensis [GC]) and social Mahali mole-rat (Cryptomys hottentotus mahali [CHM]), to varying Ta cycles in the absence of light. We showed that the LA rhythms of these two species entrain to Ta cycles and that the majority of LA occurred during the coolest 12-h period. LA confined to the coolest Ta periods may be the direct consequence of the poor heat dissipation abilities of African mole-rats brought about by physiological and ecological constraints. Recently, it has been hypothesized that Ta is only a strong zeitgeber for circadian rhythms in species whose thermoregulatory abilities are sensitive to changes in Ta (i.e., heterotherms and ectotherms), which previously has excluded endothermic-homeothermic mammals. However, this study demonstrates that Ta is a strong zeitgeber or entrainer for circadian rhythms of LA in subterranean endothermic-homeothermic mammals as a consequence of their sensitivity to changes in Ta brought about by their poor heat dissipation abilities. This study reinforces the intimate link between circadian rhythms and thermoregulation and conclusively, for the first time, provides evidence that Ta is a strong zeitgeber for endothermic-homeothermic mammals.

Bone remodeling in the longest living rodent, the naked mole-rat: Interelement variation and the effects of reproduction.

The pattern of bone remodeling of one of the most peculiar mammals in the world, the naked mole-rat (NMR), was assessed. NMRs are known for their long lifespans among rodents and for having low metabolic rates. We assessed long-term in vivo bone labeling of subordinate individuals, as well as the patterns of bone resorption and bone remodeling in a large sample including reproductive and non-reproductive individuals (n = 70). Over 268 undecalcified thin cross-sections from the midshaft of humerus, ulna, femur and tibia were analyzed with confocal fluorescence and polarized light microscopy. Fluorochrome analysis revealed low osteogenesis, scarce bone resorption and infrequent formation of secondary osteons (Haversian systems) (i.e., slow bone turnover), thus most likely reflecting the low metabolic rates of this species. Secondary osteons occurred regardless of reproductive status. However, considerable differences in the degree of bone remodeling were found between breeders and non-breeders. Pre-reproductive stages (subordinates) exhibited quite stable skeletal homeostasis and bone structure, although the attainment of sexual maturity and beginning of reproductive cycles in female breeders triggered a series of anabolic and catabolic processes that up-regulate bone turnover, most likely associated with the increased metabolic rates of reproduction. Furthermore, bone remodeling was more frequently found in stylopodial elements compared to zeugopodial elements. Despite the limited bone remodeling observed in NMRs, the variation in the pattern of skeletal homeostasis (interelement variation) reported here represents an important aspect to understand the skeletal dynamics of a small mammal with low metabolic rates. Given the relevance of the remodeling process among mammals, this study also permitted the comparison of such process with the well-documented histomorphology of extinct therapsids (i.e., mammalian precursors), thus evidencing that bone remodeling and its endocortical compartmentalization represent ancestral features among the lineage that gave rise to mammals. It is concluded that other factors associated with development (and not uniquely related to biomechanical loading) can also have an important role in the development of bone remodeling.

Long bone histomorphogenesis of the naked mole-rat: Histodiversity and intraspecific variation.

Lacking fur, living in eusocial colonies and having the longest lifespan of any rodent, makes naked mole-rats (NMRs) rather peculiar mammals. Although they exhibit a high degree of polymorphism, skeletal plasticity and are considered a novel model to assess the effects of delayed puberty on the skeletal system, scarce information on their morphogenesis exists. Here, we examined a large ontogenetic sample (n = 76) of subordinate individuals to assess the pattern of bone growth and bone microstructure of fore- and hindlimb bones by using histomorphological techniques. Over 290 undecalcified thin cross-sections from the midshaft of the humerus, ulna, femur, and tibia from pups, juveniles and adults were analyzed with polarized light microscopy. Similar to other fossorial mammals, NMRs exhibited a systematic cortical thickening of their long bones, which clearly indicates a conserved functional adaptation to withstand the mechanical strains imposed during digging, regardless of their chisel-tooth predominance. We describe a high histodiversity of bone matrices and the formation of secondary osteons in NMRs. The bones of pups are extremely thin-walled and grow by periosteal bone formation coupled with considerable expansion of the medullary cavity, a process probably tightly regulated and adapted to optimize the amount of minerals destined for skeletal development, to thus allow the female breeder to produce a higher number of pups, as well as several litters. Subsequent cortical thickening in juveniles involves high amounts of endosteal bone apposition, which contrasts with the bone modeling of other mammals where a periosteal predominance exists. Adults have bone matrices predominantly consisting of parallel-fibered bone and lamellar bone, which indicate intermediate to slow rates of osteogenesis, as well as the development of poorly vascularized lamellar-zonal tissues separated by lines of arrested growth (LAGs) and annuli. These features reflect the low metabolism, low body temperature and slow growth rates reported for this species, as well as indicate a cyclical pattern of osteogenesis. The presence of LAGs in captive individuals was striking and indicates that postnatal osteogenesis and its consequent cortical stratification most likely represents a plesiomorphic thermometabolic strategy among endotherms which has been suggested to be regulated by endogenous rhythms. However, the generalized presence of LAGs in this and other subterranean taxa in the wild, as well as recent investigations on variability of environmental conditions in burrow systems, supports the hypothesis that underground environments experience seasonal fluctuations that may influence the postnatal osteogenesis of animals by limiting the extension of burrow systems during the unfavorable dry seasons and therefore the finding of food resources. Additionally, the intraspecific variation found in the formation of bone tissue matrices and vascularization suggested a high degree of developmental plasticity in NMRs, which may help explaining the polymorphism reported for this species. The results obtained here represent a valuable contribution to understanding the relationship of several aspects involved in the morphogenesis of the skeletal system of a mammal with extraordinary adaptations.

Risk assessment in the plateau pika (Ochotona curzoniae): intensity of behavioral response differs with predator species.

BACKGROUND: The ability of a prey species to assess the risk that a predator poses can have important fitness advantages for the prey species. To better understand predator-prey interactions, more species need to be observed to determine how prey behavioral responses differ in intensity when approached by different types of predators. The plateau pika (Ochotona curzoniae) is preyed upon by all predators occurring in its distribution area. Therefore, it is an ideal species to study anti-predator behavior. In this study, we investigated the intensity of anti-predator behavior of pikas in response to visual cues by using four predator species models in Maqu County on the eastern Qinghai-Tibetan Plateau. RESULTS: The behavioral response metrics, such as Flight Initiation Distance (FID), the hiding time and the percentage of vigilance were significantly different when exposed to a Tibetan fox, a wolf, a Saker falcon and a large-billed crow, respectively. Pikas showed a stronger response to Saker falcons compared to any of the other predators. CONCLUSIONS: Our results showed that pikas alter their behavioral (such as FID, the hiding time and the vigilance) response intensity to optimally balance the benefits when exposed to different taxidermy predator species models. We conclude that pikas are able to assess their actual risk of predation and show a threat-sensitive behavioral response.

The effect of varying laboratory conditions on the locomotor activity of the nocturnal Namaqua rock mouse (Micaelamys namaquensis) and the diurnal Four-striped grass mouse (Rhabdomys dilectus).

Rodents are the most common laboratory animals all over the world, however, most studies on the effects of laboratory conditions on the behavior and physiology of the study animals have been performed on traditional laboratory animals. We investigated the effects of environmental enrichment, lighting conditions and ambient temperature cycles on the locomotor activity of wild trapped, nocturnal Namaqua rock mice and diurnal Four-striped grass mice. When considering the general activity of the two species, the diurnal species showed more variability in locomotor activity than the nocturnal species. Cage enrichment differentially affected the intensity of the locomotor activity in the two species. Despite a decrease in activity, the diurnal species showed more structured rhythms in an enriched cage. Twilight conditions changed the behavior of both species, the active time of the nocturnal animal was contracted to the completely dark hours of the light cycle, while the active time of the diurnal species was extended in the longer daylight hours. The natural light appears to stabilize the entrainment of the diurnal species. The natural ambient temperature cycle caused changes in intensity of activity, but reinforced entrainment in both species. These results show that changes in laboratory housing conditions can affect the activity of captive wild animals and that these effects are species specific. By increasing our understanding of the effects of different environmental factors on the outcomes of experiments, both the results obtained, and the welfare of the captive animals may be improved.

Exploratory behaviour, memory and neurogenesis in the social Damaraland mole-rat (Fukomys damarensis).

Both exploratory behaviour and spatial memory are important for survival in dispersing animals. Exploratory behaviour is triggered by novel environments and having a better spatial memory of the surroundings provides an adaptive advantage to the animals. Spatial challenges can also affect neurogenesis in the hippocampus by increasing cell proliferation and enhancing survival of young neurons. In social Damaraland mole-rat colonies, the social hierarchy is largely based on body size. Individuals with different social statuses in these colonies display different dispersal behaviours and as behavioural differences have been linked to dispersal behaviour, I investigated exploratory behaviour, memory and hippocampal neurogenesis in wild-captured Damaraland mole-rats. Dispersal behaviour gives rise to differential exploratory behaviour in Damaraland mole-rats; they readily explored in a novel environment but resident, worker mole-rats explored more slowly. In the Y-maze, animals entered the escape hole significantly faster by the second day; however, they did not make fewer wrong turns with successive days of the experiment. Female dispersers did not show any improvement in time to reach the escape hole or the number of wrong turns over the 4 day experimental period. Damaraland male and female dispersers employ different dispersal strategies, and this is evident in their approach to the learning task. Females are less motivated to complete the task, leading to a difference in behaviour, and this has important survival implications for the different sexes. Finally, in the context of memory, adult neurogenesis does not seem to be a good marker in mole-rats as it is generally low and has not been investigated thoroughly enough to determine which and how other factors can influence it in these animals.

Effect of colony disruption and social isolation on naked mole-rat endocrine correlates.

The social environment of animals can have profound implications on their behaviour and physiology. Naked mole-rats (Heterocephalus glaber) are highly social with complex dominance hierarchies that influence both stress- and reproduction-related hormones. Homeostasis may be affected by aggressive interactions, colony instability and social isolation. Furthermore, naked mole-rat colonies are characterised by a marked reproductive skew; a single female and few males are reproductively active while other colony members are reproductively suppressed. Thus, there are distinct differences in related hormone concentrations between reproductively active and non-active animals; however, this changes when non-reproductive individuals are removed from the colony. We investigated the effects of social isolation and colony disruption on plasma cortisol and progesterone concentrations in non-breeding naked mole-rats. During colony disruption, we found a significant increase in cortisol concentrations in females removed from the colony for social isolation (experimental) as well as in females that remained in the colony (control). Cortisol concentrations were reduced in both groups after experimental animals were paired up. No changes in cortisol concentrations were observed in control or experimental males after removal from the colony or pairing. This suggests that the females, but not the males, found colony disruption and social isolation stressful. Upon removal from the colony, both control and experimental females showed a small increase in progesterone, which returned to basal levels again in the control animals. Experimental females showed a dramatic spike in progesterone when they were paired with males, indicating reproductive activation. The sex difference in the stress responses may be due to the stronger reproductive suppression imposed on females, or the increased likelihood of dispersal for males. It is clear that the social environment reflects on the endocrine correlates of animals living in a colony, and that the colony structure may affect the sensitivity of the animals to changes in their environment.

Effects of the colour of photophase light on locomotor activity in a nocturnal and a diurnal South African rodent.

Many physiological and behavioural responses to varying qualities of light, particularly during the night (scotophase), have been well documented in rodents. We used varying wavelengths of day-time (photophase) lighting to assess daily responses in locomotor activity in the nocturnal Namaqua rock mouse (Micaelamys namaquensis) and diurnal four-striped field mouse (Rhabdomys pumilio). Animals were exposed to three light-dark cycle regimes: a short-wavelength- (SWLC, blue), a medium-wavelength- (MWLC, green) and a long-wavelength light-dark cycle (LWLC, red). Overall, daily locomotor activity of both species changed according to different wavelengths of light: the diurnal species displayed most activity under the SWLC and the nocturnal species exhibited the highest levels of activity under the LWLC. Both species showed an increase in diurnal activity and a decrease in nocturnal activity under the LWLC. These results indicate an attenuated responsiveness to long-wavelength light in the nocturnal species, but this does not appear to be true for the diurnal species. These results emphasize that the effect of light on the locomotor activity of animals depends on both the properties of the light and the temporal organization of activity of a species.

Locomotor activity and body temperature rhythms in the Mahali mole-rat (C. h. mahali): The effect of light and ambient temperature variations.

African mole-rats (family: Bathyergidae) are strictly subterranean mammals that reside in extensive networks of underground tunnels. They are rarely, if ever, exposed to light and experience muted temperature ranges. Despite these constant conditions, the presence of a functional circadian clock capable of entraining to external light cues has been reported for a number of species. In this study, we examine a social mole-rat species, Cryptomys hottentotus mahali, to determine if it possesses a functional circadian clock that is capable of perceiving light and ambient temperature cycles, and can integrate these cues into circadian rhythms of locomotor activity and core body temperature. Eight male and eight female, non-reproductive individuals were subjected to six cycles of varying light and temperature regimes. The majority of the individuals displayed daily rhythms of locomotor activity and body temperature that are synchronised to the external light and temperature cycles. Furthermore, endogenous rhythms of both locomotor activity and core body temperature were displayed under constant conditions. Thus, we can conclude that C. h. mahali possesses a functional circadian clock that can integrate external light and temperature cues into circadian rhythms of locomotor activity and core-body temperature.

Specialized mechanoreceptor systems in rodent glabrous skin.

KEY POINTS: An ex vivo preparation was developed to record from single sensory fibres innervating the glabrous skin of the mouse forepaw. The density of mechanoreceptor innervation of the forepaw glabrous skin was found to be three times higher than that of hindpaw glabrous skin. Rapidly adapting mechanoreceptors that innervate Meissner's corpuscles were severalfold more responsive to slowly moving stimuli in the forepaw compared to those innervating hindpaw skin. We found a distinct group of small hairs in the centre of the mouse hindpaw glabrous skin that were exclusively innervated by directionally sensitive D-hair receptors. The directional sensitivity, but not the end-organ anatomy, were the opposite to D-hair receptors in the hairy skin. Glabrous skin hairs in the hindpaw are not ubiquitous in rodents, but occur in African and North American species that diverged more than 65 million years ago. ABSTRACT: Rodents use their forepaws to actively interact with their tactile environment. Studies on the physiology and anatomy of glabrous skin that makes up the majority of the forepaw are almost non-existent in the mouse. Here we developed a preparation to record from single sensory fibres of the forepaw and compared anatomical and physiological receptor properties to those of the hindpaw glabrous and hairy skin. We found that the mouse forepaw skin is equipped with a very high density of mechanoreceptors; >3 times more than hindpaw glabrous skin. In addition, rapidly adapting mechanoreceptors that innervate Meissner's corpuscles of the forepaw were severalfold more sensitive to slowly moving mechanical stimuli compared to their counterparts in the hindpaw glabrous skin. All other mechanoreceptor types as well as myelinated nociceptors had physiological properties that were invariant regardless of which skin area they occupied. We discovered a novel D-hair receptor innervating a small group of hairs in the middle of the hindpaw glabrous skin in mice. These glabrous skin D-hair receptors were direction sensitive albeit with an orientation sensitivity opposite to that described for hairy skin D-hair receptors. Glabrous skin hairs do not occur in all rodents, but are present in North American and African rodent species that diverged more than 65 million years ago. The function of these specialized hairs is unknown, but they are nevertheless evolutionarily very ancient. Our study reveals novel physiological specializations of mechanoreceptors in the glabrous skin that likely evolved to facilitate tactile exploration.

The topography of rods, cones and intrinsically photosensitive retinal ganglion cells in the retinas of a nocturnal (Micaelamys namaquensis) and a diurnal (Rhabdomys pumilio) rodent.

We used immunocytochemistry to determine the presence and topographical density distributions of rods, cones, and intrinsically photosensitive retinal ganglion cells (ipRGCs) in the four-striped field mouse (Rhabdomys pumilio) and the Namaqua rock mouse (Micaelamys namaquensis). Both species possessed duplex retinas that were rod dominated. In R. pumilio, the density of both cones and rods were high (cone to rod ratio: 1:1.23) and reflected the species' fundamentally diurnal, but largely crepuscular lifestyle. Similarly, the ratio of cones to rods in M. namaquensis (1:12.4) reflected its nocturnal lifestyle. Similar rod density peaks were observed (R. pumilio: ~84467/mm2; M. namaquensis: ~81088/mm2), but a density gradient yielded higher values in the central (~56618/mm2) rather than in the peripheral retinal region (~32689/mm2) in R. pumilio. Two separate cone types (S-cones and M/L-cones) were identified implying dichromatic color vision in the study species. In M. namaquensis, both cone populations showed a centro-peripheral density gradient and a consistent S- to M/L-cone ratio (~1:7.8). In R. pumilio, S cones showed a centro-peripheral gradient (S- to M/L-cone ratio; central: 1:7.8; peripheral: 1:6.8) which appeared to form a visual streak, and a specialized area of M/L-cones (S- to M/L-cone ratio: 1:15) was observed inferior to the optic nerve. The number of photoreceptors per linear degree of visual angle, estimated from peak photoreceptor densities and eye size, were four cones and 15 rods per degree in M. namaquensis and 11 cones and 12 rods per degree in R. pumilio. Thus, in nocturnal M. namaquensis rods provide much finer image sampling than cones, whereas in diurnal/crepuscular R. pumilio both photoreceptor types provide fine image sampling. IpRGCs were comparably sparse in R. pumilio (total = 1012) and M. namaquensis (total = 862), but were homogeneously distributed in M. namaquensis and densest in the dorso-nasal quadrant in R. pumilio. The adaptive significance of the latter needs further investigation.

Analysis of gonadotrophin-releasing hormone-1 and kisspeptin neuronal systems in the nonphotoregulated seasonally breeding eastern rock elephant-shrew (Elephantulus myurus).

Of the 18 sub-Saharan elephant-shrew species, only eastern rock elephant-shrews reproduce seasonally throughout their distribution, a process seemingly independent of photoperiod. The present study characterizes gonadal status and location/intensity of gonadotrophin-releasing hormone-1 (GnRH-1) and kisspeptin immunoreactivities in this polyovulating species in the breeding and nonbreeding seasons. GnRH-1-immunoreactive (ir) cell bodies are predominantly in the medial septum, diagonal band, and medial preoptic area; processes are generally sparse except in the external median eminence. Kisspeptin-ir cell bodies are detected only within the arcuate nucleus; the density of processes is generally low, except in the septohypothalamic nucleus, ventromedial bed nucleus of the stria terminalis, arcuate nucleus, and internal and external median eminence. Kisspeptin-ir processes are negligible at locations containing GnRH-1-ir cell bodies. The external median eminence is the only site with conspicuously overlapping distributions of the respective immunoreactivities and, accordingly, a putative site for kisspeptin's regulation of GnRH-1 release in this species. In the nonbreeding season in males, there is an increase in the rostral population of GnRH-1-ir cell bodies and density of GnRH-1-ir processes in the median eminence. In both sexes, the breeding season is associated with increased kisspeptin-ir process density in the rostral periventricular area of the third ventricle and arcuate nucleus; at the latter site, this is positively correlated with gonadal mass. Cross-species comparisons lead us to hypothesize differential mechanisms within these peptidergic systems: that increased GnRH-1 immunoreactivity during the nonbreeding season reflects increased accumulation with reduced release; that increased kisspeptin immunoreactivity during the breeding season reflects increased synthesis with increased release.

From Mice to Mole-Rats: Species-Specific Modulation of Adult Hippocampal Neurogenesis.

Rodent populations living in their natural environments have very diverse ecological and life history profiles that may differ substantially from that of conventional laboratory rodents. Free-living rodents show species-specific neurogenesis that are dependent on their unique biology and ecology. This perspective aims to illustrate the benefit of studying wild rodent species in conjunction with laboratory rodents. African mole-rats are discussed in terms of habitat complexity, social structures, and longevity. African mole-rats are a group of subterranean rodents, endemic to Africa, that show major differences in both intrinsic and extrinsic traits compared to the classical rodent models. Mole-rats exhibit a spectrum of sociality within a single family, ranging from solitary to eusocial. This continuum of sociality provides a platform for comparative testing of hypotheses. Indeed, species differences are apparent both in learning ability and hippocampal neurogenesis. In addition, social mole-rat species display a reproductive division of labor that also results in differential hippocampal neurogenesis, independent of age, offering further scope for comparison. In conclusion, it is evident that neurogenesis studies on conventional laboratory rodents are not necessarily representative, specifically because of a lack of diversity in life histories, uniform habitats, and low genetic variability. The observed level of adult neurogenesis in the dentate gyrus is the result of an intricate balance between many contributing factors, which appear to be specific to distinct groups of animals. The ultimate understanding of the functional and adaptive role of adult neurogenesis will involve research on both laboratory animals and natural rodent populations.

Effects of photophase illuminance on locomotor activity, urine production and urinary 6-sulfatoxymelatonin in nocturnal and diurnal South African rodents.

Effects of photophase illuminance (1, 10, 100 and 330 lx of white incandescent lighting) on daily rhythms of locomotor activity, urine production and 6-sulfatoxymelatonin (6-SMT; 10 versus 330 lx) were studied in nocturnal Namaqua rock mice (Micaelamys namaquensis) and diurnal four-striped field mice (Rhabdomys pumilio). Micaelamys namaquensis was consistently nocturnal (∼90-94% nocturnal activity), whereas considerable individual variation marked activity profiles in R. pumilio, but with activity mostly pronounced around twilight (∼55-66% diurnal activity). The amplitude of daily activity was distinctly affected by light intensity and this effect was greater in M. namaquensis than in R. pumilio Only M. namaquensis displayed a distinctive daily rhythm of urine production, which correlated with its activity rhythm. Mean daily urine production appeared to be attenuated under dim photophase conditions, particularly in R. pumilio The results suggest that the circadian regulation of locomotor activity and urine production possesses separate sensitivity thresholds to photophase illuminance. Micaelamys namaquensis expressed a significant daily 6-SMT rhythm that peaked during the late night, but the rhythm was attenuated by the brighter photophase cycle (330 lx). Rhabdomys pumilio appeared to express an ultradian 6-SMT rhythm under both lighting regimes with comparable mean daily 6-SMT values, but with different temporal patterns. It is widely known that a natural dark phase which is undisturbed by artificial light is essential for optimal circadian function. Here, we show that light intensity during the photophase also plays a key role in maintaining circadian rhythms in rodents, irrespective of their temporal activity rhythm.

Locomotor Activity and Body Temperature Patterns over a Temperature Gradient in the Highveld Mole-Rat (Cryptomys hottentotus pretoriae).

African mole-rats are strictly subterranean mammals that live in extensive burrow systems. High humidity levels in the burrows prevent mole-rats from thermoregulating using evaporative cooling. However, the relatively stable environment of the burrows promotes moderate temperatures and small daily temperature fluctuations. Mole-rats therefore display a relatively wide range of thermoregulation abilities. Some species cannot maintain their body temperatures at a constant level, whereas others employ behavioural thermoregulation. Here we test the effect of ambient temperature on locomotor activity and body temperature, and the relationship between the two parameters, in the highveld mole-rat. We exposed mole-rats to a 12L:12D and a DD light cycle at ambient temperatures of 30°C, 25°C and 20°C while locomotor activity and body temperature were measured simultaneously. In addition, we investigated the endogenous rhythms of locomotor activity and body temperature at different ambient temperatures. Mole-rats displayed nocturnal activity at all three ambient temperatures and were most active at 20°C, but least active at 30°C. Body temperature was highest at 30°C and lowest at 20°C, and the daily cycle was highly correlated with locomotor activity. We show that the mole-rats have endogenous rhythms for both locomotor activity and body temperature. However, the endogenous body temperature rhythm appears to be less robust compared to the locomotor activity rhythm. Female mole-rats appear to be more sensitive to temperature changes than males, increased heterothermy is evident at lower ambient temperatures, whilst males show smaller variation in their body temperatures with changing ambient temperatures. Mole-rats may rely more heavily on behavioural thermoregulation as it is more energy efficient in an already challenging environment.

Sociality and the telencephalic distribution of corticotrophin-releasing factor, urocortin 3, and binding sites for CRF type 1 and type 2 receptors: A comparative study of eusocial naked mole-rats and solitary Cape mole-rats.

Various aspects of social behavior are influenced by the highly conserved corticotrophin-releasing factor (CRF) family of peptides and receptors in the mammalian telencephalon. This study has mapped and compared the telencephalic distribution of the CRF receptors, CRF1 and CRF2 , and two of their ligands, CRF and urocortin 3, respectively, in African mole-rat species with diametrically opposed social behavior. Naked mole-rats live in large eusocial colonies that are characterized by exceptional levels of social cohesion, tolerance, and cooperation in burrowing, foraging, defense, and alloparental care for the offspring of the single reproductive female. Cape mole-rats are solitary; they tolerate conspecifics only fleetingly during the breeding season. The telencephalic sites at which the level of CRF1 binding in naked mole-rats exceeds that in Cape mole-rats include the basolateral amygdaloid nucleus, hippocampal CA3 subfield, and dentate gyrus; in contrast, the level is greater in Cape mole-rats in the shell of the nucleus accumbens and medial habenular nucleus. For CRF2 binding, the sites with a greater level in naked mole-rats include the basolateral amygdaloid nucleus and dentate gyrus, but the septohippocampal nucleus, lateral septal nuclei, amygdalostriatal transition area, bed nucleus of the stria terminalis, and medial habenular nucleus display a greater level in Cape mole-rats. The results are discussed with reference to neuroanatomical and behavioral studies of various species, including monogamous and promiscuous voles. By analogy with findings in those species, we speculate that the abundance of CRF1 binding in the nucleus accumbens of Cape mole-rats reflects their lack of affiliative behavior.