Life expectancy, family constellation and stress in giant mole-rats (Fukomys mechowii).

Giant mole-rats (Fukomys mechowii) are remarkably long-lived subterranean rodents (maximum recorded lifespan as reported here greater than 26 years) that live in families with one reproductive pair (breeders) and their non-reproductive offspring (non-breeders). Previous studies have shown that breeders live on average approximately twice as long as non-breeders, a finding contradicting the classic trade-off between reproduction and lifespan. Because recent evidence points to the hypothalamic-pituitary-adrenal axis as playing an important role in shaping the pace of ageing in mole-rats, we analysed the influence of the social environment of giant mole-rats on intrafamilial aggression levels, indicators of long-term stress, and, ultimately, mortality. Behavioural data indicated that family constellation, especially the presence or the absence of parents, influences agonistic behaviour. As a measure of long-term stress, we established a non-invasive method of extracting and measuring cortisol from hair of giant mole-rats. Interestingly, orphaned non-breeders exhibited significantly lower levels of cortisol and lower mortality rates than did non-breeders living with both parents. Because hypercortisolism is harmful in the long-term, intrafamilial stress could help explain the earlier onset of senescence in non-breeders, resulting in a shorter lifespan. Our findings suggest that the social environment should be considered as a further factor in ageing studies involving group-living animals. This article is part of the theme issue 'Ageing and sociality: why, when and how does sociality change ageing patterns?'

Further support for the alignment of cattle along magnetic field lines: reply to Hert et al.

Hert et al. (J Comp Physiol A, 2011) challenged one part of the study by Begall et al. (PNAS 105:13451-13455, 2008) claiming that they could not replicate the finding of preferential magnetic alignment of cattle recorded in aerial images of Google Earth. However, Hert and co-authors used a different statistical approach and applied the statistics on a sample partly unsuitable to examine magnetic alignment. About 50% of their data represent noise (resolution of the images is too poor to enable unambiguous measurement of the direction of body axes, pastures are on slopes, near settlements or high voltage power-lines, etc.). Moreover, the authors have selected for their analysis only ~ 40% of cattle that were present on the pastures analyzed. Here, we reanalyze all usable data and show that cattle significantly align their body axes in North-South direction on pastures analyzed by Hert and co-authors. This finding thus supports our previous study. In addition, we show by using aerial Google Earth images with good resolution, that the magnetic alignment is more pronounced in resting than in standing cattle.

Emmonsiosis of subterranean rodents (Bathyergidae, Spalacidae) in Africa and Israel.

The presence of adiaspores of the fungal genus Emmonsia was examined in the lungs of 85 mole rats representing 3 subterranean genera: blind mole rats (Spalax galili and S. golani) from Israel, Ansell's mole-rats (Cryptomys anselli) from Zambia, and silvery mole-rats (Heliophobius argenteocinereus) from Malawi and Zambia. Emmonsiosis was found in 28% of the blind mole rats, 100% of the Ansell's mole-rats, but in none of the silvery mole-rats. Infection in African mole-rats was caused by Emmonsia parva, and infection in Israeli blind mole rats was caused by E. parva and E. crescens. The study indicates that the perennial burrow system of the Ansell's mole-rat forms an appropriate microhabitat for the saprophytic growth of E. parva in Lusaka region, Zambia. We suggest that factors contributing to the striking difference in prevalence of emmonsiosis between the two African mole-rat genera (Cryptomys, Heliophobius) may be their differing burrow types, burrow longevity, and social lives.

Neuroanatomy of magnetoreception: the superior colliculus involved in magnetic orientation in a mammal.

The neural substrate subserving magnetic orientation is largely unknown in vertebrates and unstudied in mammals. We combined a behavioral test for magnetic compass orientation in mole rats and immunocytochemical visualization of the transcription factor c-Fos as a marker of neuronal activity. We found that the superior colliculus of the Zambian mole rat (Cryptomys anselli) contains neurons that are responsive to magnetic stimuli. These neurons are directionally selective and organized within a discrete sublayer. Our results constitute evidence for the involvement of a specific mammalian brain structure in magnetoreception.

Visual system labeled by c-Fos immunohistochemistry after light exposure in the 'blind' subterranean zambian mole-rat (Cryptomys anselli).

The Zambian mole-rat (Cryptomys anselli) is a rodent that lives and forages underground, and under natural conditions is rarely, if ever, exposed to light. Its eye is organized as in other rodents and is prominent but minuscule. The animals do not seem to react to light behaviorally or to orient visually, although exact physiological and/or behavioral experiments have not been conducted to date. Nuclear expression of transcriptional regulatory protein (c-Fos) as a marker of cell activity was studied immunohistochemically in five mole-rats exposed to bright light for 1 h after 3 days in constant darkness, and in four non-stimulated control animals that were kept in darkness for three days and then killed under deep anesthesia. The retinae and retino-recipient areas of non-stimulated animals remained unlabeled, but many of these structures showed strong c-Fos expression bilaterally [retina, dorsal lateral geniculate body (DLG), olivary pretectal nucleus, retrosplenial cortex, neocortex] in light-exposed animals. In contrast, the suprachiasmatic nucleus did not seem to be affected by light stimuli during the experiment. In both light-stimulated and control animals the rudimentary superior colliculus exhibited slight immunoreactivity. Interestingly, the olivary pretectal nucleus, which in mammals is involved in light/dark discrimination, as well as the DLG as part of the image-forming visual system were consistently labeled by c-Fos after light stimulation, indicating that vision in Cryptomys possibly plays a more significant role than previously assumed.

Unilateral absence of the terminal nerve and distribution of gonadotropin-releasing hormone immunoreactive neurons in the brain of the common mole-rat (Cryptomys, Rodentia).

A paired terminal nerve with gonadotropin-releasing hormone-immunoreactive (GnRHir) neurons was found in five of six specimens of the Zambian common mole-rat (Cryptomys sp.). In these animals the distribution of GnRHir neurons in the CNS was approximately even on both sides. One adult female lacked a right terminal nerve, yet exhibited a comparable total number of GnRHir neurons, most of which were located on the left side of the brain, i. e., on that side where the terminal nerve was present. An additional population of GnRHir cells was detected in the area of the parafascicular and dorsomedial thalamic nuclei of three non-reproductive adult females, but not in young animals (one female, two males). The additional GnRHir cells, referred to as dark spot cells (DSCs) since their perikarya exhibit large or small strongly immunoreactive vacuoles, were present on both sides of the brain in equal numbers even in the specimen with unilateral absence of the terminal nerve. Obviously, the lack of one terminal nerve correlates with a drastic reduction in the number of ipsilateral genuine neurons but leaves the DSCs unaffected.

Ovarian growth and folliculogenesis in breeding and nonbreeding females of a social rodent, the Zambian common mole-rat, Cryptomys sp.

Zambian common mole-rats are subterranean rodents that live in families with only one female breeding. Her offspring remain in the parental nest and do not reproduce. Behavioral experiments (Burda, '95) demonstrated that their apparent "sterility" is based on incest avoidance and individual recognition of family members. To elucidate whether some kind of morphologically apparent ovarian suppression still takes place in daughters, ovaries of females of known age, weight, and reproductive histories were examined histologically and morphometrically. The body mass of old females (more than 3 years of age) begins to decrease, and the ovaries seem to begin to atrophy at the age of about 3-6 years. Ovaries in neonates exhibited primordial and primary follicles, sometimes clustered in nests. Ovaries of adult nonbreeding females expressed all stages of the follicular development up to tertiary follicles. Many unruptured luteinized follicles were present, but true corpora lutea as a morphological sign of ovulation were missing. Unruptured luteinized follicles also could be found (additionally to true corpora lutea) in ovaries of breeding females. The number of primordial follicles dropped rapidly during the first 2 years of age; the number of primary, secondary, and tertiary follicles was subject to individual variation; and there was no clear correlation with age or reproductive status. While a tendency to form accessory unruptured luteinized follicles may just reflect taxonomic affinities of bathyergids to hystricomorphs, the otherwise complete folliculogenesis in "sterile" daughters and the presence of unruptured luteinized follicles even in breeding females are further evidence that there is no hormonal suppression of the ovarial cycle. We suggest that ovulation in nonbreeding females is not actively suppressed by the breeding female, but instead that it is not released because the triggering mechanisms, most probably repeated copulation, are missing.

Adaptive differentiations of the skin of the head in a subterranean rodent, Spalax ehrenbergi.

The skin of macroscopically distinct regions (hairy skin, vibrissal fields, buccal ridge, and rhinarium) of the head of the blind mole-rat, Spalax ehrenbergi, was studied by routine histological methods. Few guard and several soft vellus hairs are organized into tufts that grow from a group of hair follicles localized in an invaginated compound cavity. We suggest that this hair arrangement may be a burrowing adaptation to match frictional resistance. The follicles and the compound cavity possess either well developed complex striated musculature or errector pili muscles. There are no structural specializations (sweat glands, glomus bodies) to enhance thermoregulatory (heat dissipative) capacities in the hairy skin of the head. Vibrissae penetrate the epidermal surface as single hairs. They are microscopically normally developed and arranged in vibrissal fields according to a basal mammalian pattern. Most of them are, however, relatively short and inconspicuous. The mystacial vibrissal field is horizontally divided by a prominent buccal ridge which is probably involved in bulldozing. The hairs in the ridge leave the compound cavity singularly. The follicles of guard hairs and bristles are equipped with well developed pilo-Ruffini complexes indicating that the buccal ridge may serve also as a tactile organ. The glabrous skin of the rhinarium has a highly interdigitated dermal-epidermal interface. The dermal papillae possess simple lamellated and/or simple Meissner's corpuscles and few Merkel cell-axon-complexes indicating that the skin of the rhinarium may be particularly sensitive to perception of vibrations.

Hearing in blind subterranean Zambian mole-rats (Cryptomys sp.): collective behavioural audiogram in a highly social rodent.

Thresholds for pure tone detection were examined in the common mole-rat, Cryptomys sp. (Bath-yergidae, Rodentia) using a positive reinforcement procedure. To bypass the problems connected with testing isolated individuals of this extremely social species, a collective behavioural audiogram was determined for a family group of seven mole-rats. Within the tested frequency range of 225 to 18 kHz, the lowest thresholds (as low as 7.5 dB SPL, on average 24 dB SPL) were found at 800 Hz, the upper limit of hearing (at the level of 60 dB SPL) was at 18 kHz. The behavioural audiogram combines the results of previous studies on hearing in this species. It resembles the distortion threshold curve but differs from neurophysiological data as far as the high frequency cutoff is concerned. On the other hand, the region of the best hearing sensitivity is narrow in behavioural audiogram and neurophysiological curves but rather broad in the distortion threshold curve. In general, the behavioural audiogram of Cryptomys is in many aspects comparable with the available audiograms of other subterranean rodents.

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

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

Acoustic distortion products from the cochlea of the blind African mole rat, Cryptomys spec.

The measurement of distortion-product otoacoustic emissions is a noninvasive method that can be used for assessing the sensitivity and the frequency tuning of nonlinear cochlear mechanics. During stimulation with two pure tones f1 and f2, the acoustic 2f1-f2 distortion was recorded in the ear canal of Cryptomys spec. to study specializations in cochlear mechanics that could be associated with the presence of a frequency expanded cochlear region between 0.8-1 kHz. In addition, a distortion threshold curve was obtained which describes relative threshold of nonlinear cochlear mechanics. Sensitive distortion thresholds could be measured for stimulus frequencies between 0.4 to 18 kHz with a broad minimum between 0.75 to 2.5 kHz. The distortion threshold curve extends to higher frequencies than previous neuronal data indicated. As a measure of mechanical tuning sharpness in the cochlea, suppression tuning curves of 2f1-f2 were recorded. The tuning curves reflected the typical mammalian pattern with shallow low frequency and steep high frequency slopes. Their tuning sharpness was poor with Q10dB values between 0.3 and 1.88. In the range of the frequency expanded region, the Q10dB values were below 0.5. This finding emphasizes that the presence of frequency expansion does not necessarily lead to enhanced mechanical tuning in the cochlea and one has to consider if in certain bat species with cochlear frequency expansion and particularly sharp cochlear tuning, the two phenomena may not be interlinked.

Convergent evolution of the vestibular organ in the subterranean mole-rats, Cryptomys and Spalax, as compared with the aboveground rat, Rattus.

The membranous labyrinth of the vestibular organ (examined in toto) in two unrelated species of subterranean rodents, Cryptomys sp. from Zambia and Spalax ehrenbergi from Israel, was in many parameters (streamline length, curvature radius, and cross-sectional area of the lumen) relatively or even absolutely (especially the cross-sectional area) larger than in the laboratory Norway rat. The mechanical sensitivity of the vestibular organ (estimated according to the mathematical model of Oman et al., [1987] Acta. Otolaryngol (Stockh.) 103:1-13) was similar in both subterranean rodent species and significantly higher than that in the laboratory rat. The most pronounced differences in morphometry and the resulting mechanical sensitivity between the subterranean forms and the rat occurred in the lateral (i.e., phylogenetically and ontogenetically most recent and presumably most plastic) semicircular duct. The area of the sensory epithelia, and density and total numbers of vestibular receptors, were estimated on surface specimens for both maculae and for all three cristae for all three species. While the density of hair cells in comparable sensory epithelia was similar in all three species, the sensory area and thus, also, the total receptor counts were significantly larger in both subterranean forms. The peripheral vestibular organ in subterranean rodents is, in comparison to a generalized aboveground dwelling form, i.e., the rat, progressively specialized, and in any case cannot be denoted as degenerate.

Individual recognition and incest avoidance in eusocial common mole-rats rather than reproductive suppression by parents.

Non-reproductive females in families of eusocial common mole-rats (Cryptomys sp., Rodentia) are not suppressed by their mother, (either behaviourally or pheromonally) as is generally assumed. They do not mate with their father and brothers simply because they are not sexually attractive for them (and vice versa). The incest avoidance is based on the capability to recognize (and keep in memory for up to three weeks) each family member individually. A 'sterile' daughter may conceive and deliver young in her parental family if given the opportunity to mate with an unfamiliar mate in a separate cage. In this way, two females may breed side by side in one family.

Functional allometry of the semicircular ducts in subterranean mole-rats Cryptomys (Bathyergidae, Rodentia).

BACKGROUND: Since the spatial mobility of subterranean mole-rats is restricted and their skull strongly modified, morpho-functional regression of their vestibular organ may be expected. On the other hand, vestibular sense may be indispensable for orientation in a world deprived of most external sensory cues. Since vestibular sensitivity is determined by the size of the labyrinth, morphometrical analysis may be employed to assess the sensitivity and to test whether the organ is degenerate or progressively specialized. METHODS: We analyzed the shape and size of the membranous labyrinth of vestibular organs in toto in three species of African subterranean blind mole-rats of the genus Cryptomys (Bathyergidae) differing in body size yet not in habitats, ways of life, or employed orientation and locomotory strategies. The mechanical sensitivity of the cupula was estimated according to Oman et al. (1987. Acta Otolaryngol. (Stockh.), 103:1-13) for each of the three semicircular ducts. RESULTS: The size and shape of the vestibular organ changed predictably depending on species-specific (yet not individual) body mass. In some aspects, particularly the cross-sectional area, the ducts were larger than expected for a mammal of a comparable body size. In all species examined, the anterior semicircular ducts exhibited the highest sensitivity. CONCLUSIONS: The vestibular organs of blind subterranean mole-rats are not regressed morpho-functionally.

Morphometry of the vestibular organ in neonate and adult African mole-rats Cryptomys species.

The dimensions (length and cross-sectional area) of the semicircular canal of the inner ear in Cryptomys (a rodent with long gestation, and altricial young with slow, extended postnatal growth) did not change after birth. This is further evidence for the relative morphometric postnatal stability of semicircular structures in mammals.

Karyotype of the giant mole-rat, Cryptomys mechowi (Rodentia, Bathyergidae).

The karyotype of the giant mole-rat, Cryptomys mechowi (Rodentia, Bathyergidae), from Zambia was investigated in one male and one female by means of G-, C-, and AgNOR-banding techniques. The diploid chromosomal set consisted of 40 biarmed chromosomes (2n = 40, NF = 80). A pair of autosomes in the male and the X chromosomes in the female were heteromorphic. The sex chromosomes were unusually large.

Structure and function of the cochlea in the African mole rat (Cryptomys hottentotus): evidence for a low frequency acoustic fovea.

The cochlea of the mole rat Cryptomys hottentotus was investigated with physiological and anatomical methods. In order to reveal the place-frequency map of the cochlea, iontophoretic HRP-applications were made in the cochlear nucleus at physiologically characterized locations. Subsequent HRP-transport in auditory nerve fibres and labeling patterns of spiral ganglion cells within the cochlea were evaluated. A cochlear place-frequency map was constructed from 17 HRP-applications in the cochlear nucleus at positions where neurons had characteristic frequencies between 0.1 and 12.6 kHz. As in other mammals, high frequencies were found to be represented at the cochlear base, low frequencies at the cochlear apex. The place-frequency map had three distinct parts which were characterized by their different slopes. A clear over-representation of the frequencies between 0.6 and 1 kHz was revealed, in this frequency range the slope of the place-frequency map amounted to 5.3 mm/octave. As calculated from the regression analysis, below 0.6 kHz the slope of the cochlear place-frequency map amounted to 0.24 mm/octave, above 1 kHz to 0.9 mm/octave. As in other mammals width of the basilar membrane (BM) increased from the cochlear base towards the cochlear apex. Also in concordance with the findings in other mammals, BM-thickness decreased from the cochlear base to the apex. However, it was remarkable to find that there was no or little change in BM-width and thickness between 40 and 85% BM-length. It was also revealed that scala tympani was only 1/10th the size found in the rat or other mammals of similar body size.(ABSTRACT TRUNCATED AT 250 WORDS)

The ear in subterranean insectivora and rodentia in comparison with ground-dwelling representatives. I. Sound conducting system of the middle ear.

Compared to acoustically unspecialized mammals (soricids and murids), the middle ear of subterranean insectivores and rodents (twelve species of six families examined) was clearly distinguished and characterized by many common features: rather round and relatively larger eardrum without a pars flaccida; reduced gonial; loose or no connection between the malleus and the tympanic bone; reduced and straightened transversal part of the malleus; enlarged incus; increased and rather flat incudo-mallear joint; rather parallel position of the mallear manubrium and incudal crus longum in some species (and their fusion in bathyergids); reduced or even missing middle ear muscles. Convergent occurrence of these structural features in taxa of different origin and their generally derived character suggest that they cannot be categorized as degenerative. The form of the stapes can be considered as a non-adaptive trait; it was taxon specific yet remarkably polymorphous in some species and exhibited no convergent features among subterranean mammals. Structural retrogression resulting in a columella-like stapes was observed in some species lacking the stapedial artery. The stapedial base was relatively larger than in unspecialized mammals. The subterranean mammals did not exhibit conspicuously enlarged eardrums as would be required for sensitive tuning to low frequencies. It is, however, argued that while selective pressures in the subterranean ecotope promoted hearing of low frequencies, hearing sensitivity did not have to be enhanced.