Blind Mole Rat Spalax Research Articles

Response properties of auditory activated cells in the occipital cortex of the blind mole rat: an electrophysiological study.

Previous studies have demonstrated that despite its blindness, the subterranean blind mole rat (Spalax ehrenbergi) possesses a noticeable lateral geniculate nucleus and a typical cyto-architectural occipital cortex that are reciprocally connected. These two areas, as revealed by the metabolic tracer 2-deoxyglucose, are activated by auditory stimuli. Using single unit recordings, we show that about 57% of 325 cells located within the occipital cortex of anesthetized mole rats responded to at least one of the following auditory stimuli--white noise, pure tones, clicks, and amplitude modulated tones--with the latter two being the most effective. About 85% of cells driven by either contralateral or ipsilateral stimulation also responded to binaural stimulation; about 13% responded only to binaural stimulation; and 2% were driven exclusively by contralateral stimulation. Comparing responsiveness and response strength to these three modes of stimulation revealed a contralateral predominance. Mean latency (+/-SD) of ipsilateral and contralateral responses were 48.5+/-32.6 ms and 33.5+/-9.4 ms, respectively. Characteristic frequencies could be divided into two distinct subgroups ranging between 80 and 125 Hz and between 2,500 and 4,400 Hz, corresponding to the most intensive spectral components of the vibratory intraspecific communication signals and airborne vocalizations.

Reversed palatal perforation by upper incisors in ageing blind mole-rats (Spalax ehrenbergi).

Blind mole-rats (Spalax ehrenbergi) are fossorial solitary rodents that present striking morphological, physiological and behavioural adaptations to the subterranean environment in which they live. Previous studies have shown that mole-rats are specialised in tooth-digging. The rapid eruption-rate of their incisors has evolved to compensate for their excessive wear by excavation. Males use their incisors more than females for digging and fighting, and their rate of incisor eruption is significantly more rapid than in females. Since mole-rats use their incisors for digging throughout the year, we suggest that continuous mechanical pressure on their oral tissues concentrated at the apical sites of the upper incisors leads to cell and tissue fatigue. We provide evidence for 5 stages of palatal perforation by the upper incisors at their apical sites, with maximum perforation characterising aged males. Interspecies comparisons with 7 other fossorial and semi-fossorial rodent species, and with beavers, which expose their incisors to enormous mechanical pressure, revealed that this palatal perforation is unique to the male mole-rat. We suggest that while the fast eruption rate of incisors in the mole-rat compensates for the rapid wear resulting from digging, evolutionary adaptation to continuous tooth-digging is still ongoing, since the physical pressure of digging at the apical sites of the upper incisors leads to tissue destruction, breakage of the palatal bone and possibly to death, as a result of maxillary inflammation.

Magnetic compass orientation in the blind mole rat Spalax ehrenbergi.

The blind mole rat Spalax ehrenbergi is a solitary, subterranean rodent that digs and inhabits a system of branching tunnels, with no above-ground exits, which it never leaves unless forced to. To survive, the mole rat must be able to orient efficiently in its tunnel system. The sensory channels available for spatial orientation in the subterranean environment are restricted in comparison with those existing above ground. This study examined the possibility that the mole rat is able to perceive and use the earth's magnetic field to orient in space. Experiments were performed using a device constructed from a pair of electromagnetic 'Helmholtz coils', which create a magnetic field whose direction and strength can be altered. In the first experiment, we tested a group of mole rats (N=33) in an eight-armed maze under the earth's natural magnetic field to determine whether they have directional preferences for the location of their sleeping nest, food chamber and toilet site. A second group of mole rats (N=30) was tested for their directional preference after the earth's magnetic field had been experimentally shifted by 180 degrees. We found that the first group exhibited a significant preference (P<0.001) to build both their sleeping nest and their food store in the southern sector of the maze, whereas the second group shifted the location of their nests (P<0.01) and food store (P<0.05), to the northern sector of the maze, corresponding to the shift in the magnetic field. In the second experiment, we tested whether the magnetic compass orientation found in the first experiment depends on a light stimulus by testing a group of mole rats in the eight-armed maze under total darkness. No significant difference in directional preference between light and dark test conditions was observed. It can be concluded, therefore, that, in contrast to some amphibians and birds, magnetic compass orientation in the mole rat is independent of light stimulation. In the third experiment, we examined whether mole rats (N=24) use the earth's magnetic field as a compass cue to orient in a labyrinth. In the first stage (trials 1-13), the animals were trained to reach a goal box at the end of a complex labyrinth until all individuals had learned the task. In the second stage (trial 14), half the trained mole rats underwent another labyrinth trial under the earth's natural magnetic field, while the other half were tested under a magnetic field shifted by 180 degrees. We found a significant decrease (P<0.001) in performance of the mole rats tested under the shifted magnetic field compared with the group tested under the natural magnetic field. The findings from these experiments prove that the mole rat is able to perceive and use the earth's magnetic field to orient in space.

Noninvolvement of testosterone in aggressive defense behavior in the male blind mole ratSpalax ehrenbergi

Blind mole rats (Spalax ehrenbergi) are solitary and aggressive subterranean rodents. Aggressive defense behavior in the mole rat functions to deter neighboring competitors from territory, food, and mates and includes seismic and odor signals. The aim of the present study was to determine whether the aggressive defense behavior displayed by male mole rats is testosterone dependent. Five behavioral variables were taken as being representative of such aggressive interaction: exposing teeth, biting, bulldozing movements of the head, soil blocking, and self-grooming. We monitored male testosterone levels and aggressiveness throughout the annual cycle, which can be divided into three main climatic periods: cold and rainy (September–February); warm, during which the soil is still moist and easily excavated (March–May); and hot (June–August), when the soil is hard and dry. In a second experiment the effect of endogenous and exogenous testosterone on male aggressive defense behavior was determined before and after castration and following testosterone propionate replacement. We found fluctuations in male testosterone concentrations, with three peaks: in November, May, and August, one in each of the three climatic periods. However, these fluctuations did not correlate with male aggressive behavior, which remained constant throughout the year. Furthermore, because neither castration nor testosterone propionate replacement in castrated individuals affected their defense behavior, we suggest that such behavior in male mole rats is testosterone independent. The continuous excavation and maintenance of the mole rat’s underground tunnel system demands high energy expenditure year-round and constant defense of territory sites and food caches from intraspecific rivals. Thus, although testosterone may fluctuate as a result of seasonal breeding cycles, constant high levels of aggressive defense throughout the year are crucial for the survival of the male mole rat in its solitary subterranean environment. Aggr. Behav. 27:64–72, 2001. © 2001 Wiley-Liss, Inc.

A Fully Functional Rod Visual Pigment in a Blind Mammal: A CASE FOR ADAPTIVE FUNCTIONAL REORGANIZATION?

In the blind subterranean mole rat Spalax ehrenbergi superspecies complete ablation of the visual image-forming capability has been accompanied by an expansion of the bilateral projection from the retina to the suprachiasmatic nucleus. We have cloned the open reading frame of a visual pigment from Spalax that shows >90% homology with mammalian rod pigments. Baculovirus expression yields a membrane protein with all functional characteristics of a rod visual pigment (lambda(max) = 497 +/- 2 nm; pK(a) of meta I/meta II equilibrium = 6.5; rapid activation of transducin in the light). We not only provide evidence that this Spalax rod pigment is fully functional in vitro but also show that all requirements for a functional pigment are present in vivo. The physiological consequences of this unexpected finding are discussed. One attractive option is that during adaptation to a subterranean lifestyle, the visual system of this mammal has undergone mosaic reorganization, and the visual pigments have adapted to a function in circadian photoreception.

Effect of photoperiod variation on testes and accessory sex organs in the male blind mole rat Spalax ehrenbergi

The blind mole rat is a seasonally breeding fossorial rodent that is perceptionally blind. This study examines the effect of photoperiod on the morphology and histology of the male mole rat reproductive system. three groups of male mole rats were maintained in the laboratory under short day (SD) conditions (9L:15D); long day (LD) conditions (15L:9D); and constant darkness (CD), and compared to animals trapped in the field (FL). It was found that the field animals revealed higher testes and prostate gland weights, higher prostate tubuli volume (v *) and lower testes tubuli volume (v *) compared to the other three groups. Distribution of the tubuli in the testes (Vv) was low in the FL group compared to the SD and LD groups but still higher than in the CD group. Distribution of lumen in the testes (Vv) was higher in the CD group in comparison to the other three groups. Distribution of interstitial tissue in the testes (Vv) was higher in the FL group than in the other three groups. Electrolytes and elements secreted from the prostate gland did not differ among the four groups. In the FL group distribution of the tubuli (Vv) in the prostate gland was low and lumen ratio (Vv) was high compared to the other three groups. Distribution of connective tissue in the prostate gland did not differ among all four groups. Testosterone levels and total sperm count was highest in the FL group. Sperm production was noted in all groups; however spermatid and spermatozoa cell production was higher in the FL group. This study shows that photoperiod could be important in initiating timing in the breeding season but that certain other conditions which are absent in the laboratory appear to be responsible for successful breeding in the field.

Reproductive behavior of the blind mole-rat (Spalax ehrenbergi) in a seminatural burrow system

The blind mole-rat (Spalax ehrenbergi) is a fossorial mammal that is solitary and highly aggressive in nature. The consequent difficulties of maintaining this species in captivity have hindered attempts to gain insight into its behavior and reproductive biology. This article describes an innovative artificial tunnel system and management protocol that facilitated our study of the reproductive behavior of the blind mole-rat in captivity. The study employed a naturalistic approach that allowed the animals to establish separate territories in a seminatural tunnel system and to become familiar with each other over a period of months. This approach contrasts with previous unsuccessful attempts in which mole-rats were introduced without a period of acclimation to each other or to the experimental set-up. The results reveal that both the length of acquaintance between a pair of mole-rats and their own control of the timing of encounters are the most significant factors in reducing aggression and stress. Courtship in blind mole-rats is a lengthy process during which the animals gradually become accustomed to one another, which leads to a reduction of aggression and the initiation of positive "contact movements," eventually enabling copulation to occur. Minimal disturbance by the researcher and initiation of encounters by the mole-rats themselves appear to be the factors that led to a successful mating, pregnancy, and, 34 days later, to the female giving birth and rearing the pups in captivity.

Rest-activity rhythm of the blind mole rat Spalax ehrenbergi under different lighting conditions

The mole rat is a solitary, subterranean and photoperiodic rodent. We investigated its rest activity behavior under several lighting conditions, complemented our observations with light-induced c-fos expression, and compared the activity behavior of two chromosomal forms (2n=58 and 60). The 26 mole rats had a clear overall preference for activity in the light or dark period, but prolonged recordings in five individuals showed that the initial preference was not stable in the nocturnal animals, they became diurnal. A 6-h advance of the light-dark (LD) cycle induced a shift of activity and the previous LD preference was reestablished. The large daily variability of activity onset did not allow this study to determine whether the animals were entrained to the LD cycle upon release into constant darkness (DD) or whether activity had been masked by light. The period of the motor activity rhythm in DD free ran in more than 50% of the animals. No differences in activity were observed between the two karyotypes. Immunohistochemistry for c-fos expression in the nucleus suprachiasmaticus at different circadian times showed that c-fos was induced only in animals exposed to a 1-h light pulse during the subjective night, but not during the subjective day or in control animals in the absence of a light pulse. The large intra- and inter-individual variability in daily motor activity both in LD and in DD suggest only a weak photic entrainment of the circadian clock to light of approximately 100 lux, and possibly a weak regulation of behavior by the circadian clock.

Morphology and cytology of the nasal cavity and vomeronasal organ in juvenile and adult blind mole rats (Spalax ehrenbergi).

The blind mole rat (Spalax ehrenbergi) is a fossorial solitary rodent which exhibits extensive intraspecific aggression and uses scent markings to deter contraspecific invaders. Mole rats of different ages were captured near Tel Aviv, Israel, and sacrificed by an overdose of Xylazine hydrochloride. Olfactory epithelium sites from the nasal cavity (NC) and the vomeronasal organ (VNO) were dissected and fixed for light and electron microscopy. The mole rat's olfactory epithelium of the NC consists of several cell types, of which two types are supporting cells that comprise both microvilli and cilia but differ in staining and the presence of rough endoplasmic reticulum. The third type has no cilia. Secretory goblet cells were frequent among supporting cells of adults alone. Two types of receptor cells protrude into the NC with olfactory knobs at their apical region; one type has up to 177.6 +/- 9.4 cilia per knob plus microvilli, while the other type has only microvilli. The third type of sensory cell has no knob and contains microvilli only. The basal epithelium layer consists of short-bodied cells with round nuclei. The VNO of the mole rat is situated beneath the nasal septum, consisting of supporting, sensory, and basal cell types, with many cilia at the apical portion. At its anterior part, the VNO is connected to the NC by narrow canals. The abundance of cilia and microvilli in the mole rat olfactory cells provides the first anatomical evidence for their olfactory acuity. Such acuity is important in mole rats, compensating for their loss of vision and enabling them to detect and avoid rivals prior to potential aggressive encounters as well as to select food plants during foraging.

Ontogeny of agonistic behaviour in dispersing blind mole rats (spalax ehrenbergi)

The blind mole rat (Spalax ehrenbergi) is a solitary and aggressive fossorial rodent that inhabits its own individual tunnel system. Mole rats breed mainly in the winter, giving birth to a litter of three to four young on average [Nevo (1961) Mammalia 25:127–143]. Intraspecific interactions between adults occur mostly during the winter, which is the rainy season in Israel; after parturition, interactions occur between the mother and her offspring and between the siblings themselves until dispersal. Until now, the subterranean habitat of mole rats has prevented direct observation in the wild. Thus, there has been no direct evidence for the proximal factors that drive juvenile mole rats out of the maternal tunnel system as they shift from the social life-style of the young to the solitary life-style of the adult. In the present study, female mole rats were caught in the wild with their offspring and brought to the laboratory. The dispersal process of the young from the maternal nest was followed under two housing conditions: (1) restricted housing, simulating the physical conditions under which dispersal is delayed past the usual age, as often occurs during late winter floods in the field in areas of nonporous clay soils, and (2) nonrestricted housing, simulating the physical conditions that allow the young to disperse from their maternal tunnels at any time. In each housing condition, the mothers raised either one or three pups. During pup development, we monitored both maternal and juvenile agonistic variables during intraspecific interactions. Five major behavioural phases were identified during the ontogeny of the mole rat pups. Maternal aggression toward pups increased mainly in the first three phases of pup development, and sibling aggression increased from the third phase until dispersal. Under the restricted housing conditions, there was a delay in both the appearance of aggression in the “family group” as well as in dispersal age compared with the nonrestricted conditions. In the nonrestricted conditions, increased litter size resulted in delay in dispersal age. We suggest that the main proximate factor initiating natal dispersal is increased intolerance and aggression among siblings rather than maternal aggression. Only after the young began dispersing from the maternal tunnels did maternal aggression dramatically increase, thus preventing the offspring from returning. However, following floods, inhibition of aggression may enable the mole rat pups to stay with the family group and to disperse later when the physical conditions permit it. Aggr. Behav. 24:455–470, 1998. © 1998 Wiley-Liss, Inc.

Activity pattern and rhythm in the subterranean mole rat superspeciesSpalax ehrenbergi

Good candidates for naturally occurring variability in circadian rhythms may be subterranean herbivores, since they are not normally subjected to entraining light stimulation. To test this possibility, we selected the blind mole rat Spalax ehrenbergi superspecies in Israel and tested it in short- and long-term experiments. Short-term experiments showed that the animals exhibited three patterns of activity: a regular circadian rhythm (26.6%), an altered circadian rhythm (shorter or longer than normal, 53.1%), and an arrhythmic pattern (20.3%). A long-term experiment showed that the arrhythmic pattern indeed reflected a genuine arrhythmic genotype. The mole rats were found to be active less than 25% of the day and exhibited a multiphasic mode of activity, both diurnally and nocturnally. The number of activity periods and the level of activity were negatively correlated: Animals that exhibited a high level of activity per unit of time showed low numbers of activity periods, while animals that exhibited a lower level of activity showed higher numbers.

Cross-modal neuroplasticity in the blind mole rat Spalax ehrenbergi: a WGA-HRP tracing study.

Spalax ehrenbergi is a subterranean rodent possessing extremely degenerated eyes but a distinguishable dorsal lateral geniculate nucleus (dLGN) which projects ipsilaterally to a fair sized striate cortex. 2-Deoxyglucose and electrophysiological studies have shown that these areas are vigorously activated by auditory input. We show here, using the neuroanatomical tracer WGA-HRP, that the major source of the auditory input to the visual system is the inferior colliculus that, in addition to all its typical auditory targets, also projects to the dLGN. The visual thalamo-cortical pathway thereupon processes auditory information. This is the first naturally blind mammal in which the origin of auditory compensatory projections have been traced and described.

Seasonal activity in the blind mole rat (Spalax ehrenbergi)

The locomotor activity pattern of the blind mole rat Spalax ehrenbergi was determined in its natural habitat by means of a radiotelemetric device. Twelve adult mole rats were fitted with radiotelemetric transmitters (9 during winter and 3 during summer) and tracked for 5 noncontinuous days during which air and soil temperatures were measured. Mole rats were found to have a diurnal monophasic locomotor activity pattern with activity peaks from 08:00 to 13:00 and from 11:00 to 19:00 during summer and winter, respectively. Activity periods were punctuated by several rest breaks and, conversely, rest periods were interrupted by short spells of activity. Duration of activity was 6.6 ± 0.4 h (mean ± SD) in summer and 7.9 ± 2.3 h in winter. In the laboratory, mole rats were found to entrain their activity, under constant dim light, to a single daily 20-s light pulse. Moreover, such a light pulse given only once every 3 days was found to provide a stimulus sufficient to entrain the mole rats' locomotor activity. We propose that brief light pulses perceived through the mole rats' rudimentary eyes while they are pushing excess soil out of the tunnel to the ground surface, are the main Zeitgeber that entrains their locomotor activity to the diurnal pattern. Air and soil temperatures are the secondary cues that finely tune the activity to the morning during summer and the late afternoon during winter.

Auditory pathway and auditory activation of primary visual targets in the blind mole rat (Spalax ehrenbergi): I. 2-deoxyglucose study of subcortical centers.

The blind mole rat Spalax ehrenbergi is a subterranean rodent that shows striking behavioral, structural, and physiological adaptations to fossorial life including highly degenerated eyes and optic nerves and a behavioral audiogram that indicates high specialization for low-frequency hearing. A 2-deoxyglucose functional mapping of acoustically activated structures, in conjunction with Nissl/Klüver-Barrera-stained material, revealed a typical mammalian auditory pathway with some indications for specialized low-frequency hearing such as a poorly differentiated lateral nucleus and a well-developed medial nucleus in the superior olive complex. The most striking finding was a marked 2-deoxyglucose labeling of the dorsal lateral geniculate body and of cortical regions that correspond to visual areas in sighted rodents. The results render the blind mole rat a good model system for studying natural neural plasticity and intermodal compensation. In this report, we confine ourselves to the subcortical levels. The cortical level will be dealt comprehensively in a following paper.

Evolution of crystallins: expression of lens-specific proteins in the blind mammals mole (Talpa europaea) and mole rat (Spalax ehrenbergi).

The mole (Talpa europaea; Insectivora) and the mole rat (Spalax ehrenbergi; Rodentia) both have degenerated eyes as a convergent adaptation to subterranean life. The rudimentary eye lenses of these blind mammals no longer function in a visual process. The crystallin genes, which display a lens-specific expression pattern, were studied in these blind mammals and in related species with normal eyes by hybridizing their genomic DNAs with probes obtained from cDNA clones for alpha A-, alpha B-, and beta Bp-crystallins from calf and gamma 3-crystallin from the rat. For all crystallin genes examined, the hybridization signals of mole and mole rat genomic DNA were comparable, respectively, with those of shrew and of rat and mouse, normal-vision representatives of the orders Insectivora and Rodentia. The expression of the crystallins at the protein level was tested by using antiserum specific for alpha-crystallin in immunofluorescence reactions on lens sections of mole and mole rat eyes and by using antisera against the beta- and gamma-crystallins on sections of the mole eye. All antisera gave positive fluorescence reactions exclusively with lens tissue of these blind mammals, indicating that the crystallins are still normally expressed despite the fact that these lenses have had no function in a visual process in these mammals for at least many million years. These findings apparently imply that some unknown selective advantage has conserved the crystallin genes and their expression after the loss of normal function of the lenses.