Behavioural Tests Reveal Severe Visual Deficits in the Strictly Subterranean African Mole‐Rats (Bathyergidae) but Efficient Vision in the Fossorial Rodent Coruro (Spalacopus cyanus,Octodontidae)

Vision has long been considered purposeless in the dark underground ecotope. However, recent anatomical studies revealed an unexpected diversity of ocular and retinal features and various degrees of development of the visual system in mammals with predominantly subterranean activity, and have suggested retention of basic visual capabilities even in some strictly subterranean mammals such as the African mole‐rats. Behavioural tests assessing image‐forming vision have not yet been conducted in subterranean mammals. Here, we investigated the visual capacities in three species of the African mole‐rats, namely the giant mole‐rat Fukomys mechowii, the Mashona mole‐rat Fukomys darlingi and the silvery mole‐rat Heliophobius argenteocinereus, in the fossorial coruro Spalacopus cyanus and the inbred C57L/J mouse. The behavioural assays performed in this study revealed severe visual deficits in all three species of mole‐rats. The absence of the visual placing reflex suggested impairment of either image‐forming vision or visuomotor integration. The random choice between the shallow and the deep side of a visual cliff clearly demonstrated inability of mole‐rats to perceive depth. The nesting assay did not yield conclusive evidence regarding the capacity for visually guided spatial orientation in the only tested species, the giant mole‐rat. In contrast, both the coruro and the mouse exhibited a clear placing reaction and preferred the shallow side of the visual cliff, implying functional image‐forming vision. Thus, the behavioural data gathered in this study show that vision is seriously compromised in the strictly subterranean, congenitally microphthalmic African mole‐rats but efficient (i.e. comparable to that of surface‐dwelling rodents) in a species with regular surface activity, the coruro.     

A preliminary survey of chromosomes in populations of the Chilean burrowing octodont rodent Spalacopus cyanus Molina (Caviomorpha, Octodontidae)

Chromosomes obtained from bone-marrow, spleen and testes were studied in samples from five populations of Spalacopus cyanus of Central Chile. Animals of four low-land coastal localities and animals of a high Andean valley showed a karyotype of 2n = 58 chromosomes, with almost no variation, either in number or in structure, both within each population or among the various populations. This karyotype was found to be very similar to that of Octodon degus , but very different to those in species of Ctenomys. The evolutionary and systematic significance of these results is discussed. The lack of karyotypic variation found in Spalacopus is correlated with its taxonomic uniformity, and both could be the result of the high vagility of the populations of this rodent, suggested by previous studies. This high capacity of dispersal is supposed to have enhanced gene flow, and therewith chromosome uniformity and low taxonomic diversification. The occurrence of a case of dimorphism for the presence of a secondary constriction in one of the autosome pairs is reported and discussed.     

Acoustic communication and burrow acoustics are reflected in the ear morphology of the coruro (Spalacopus cyanus, Octodontidae), a social fossorial rodent

We studied the middle and inner ears of seven adult coruros (Spalacopus cyanus), subterranean and social rodents from central Chile, using free-hand dissection and routine staining techniques. Middle ear parameters that were focused on here (enlarged bullae and eardrums, ossicles of the "freely mobile type") are believed to enhance hearing sensitivity at lower frequencies. The organ of Corti was of a common mammalian type and revealed three peaks of higher inner hair cell densities. Based on a position frequency map, frequencies were assigned to the respective peaks along the basilar membrane. The first peak at around 300-400 Hz is discussed with respect to the burrow acoustics, while the peak around 10-20 kHz is probably a plesiomorphic feature. The most pronounced peak at around 2 kHz reflects the frequency at which the main energy of vocal communication occurs. The morphology of the ear of the coruro corresponds to the typical pattern seen in subterranean rodents (low frequency and low-sensitivity hearers), yet, at the same time, it also deviates from it in several functionally relevant features.     

When nonshivering thermogenesis equals maximum metabolic rate: thermal acclimation and phenotypic plasticity of fossorial Spalacopus cyanus (Rodentia)

Many small mammals inhabiting fluctuating and cold environments display enhanced capacity for seasonal changes in nonshivering thermogenesis (NST) and thermoregulatory maximum metabolic rate (MMR). However, it is not known how this plasticity remains in a mammal that rarely experiences extreme thermal fluctuations. In order to answer this question, we determined body mass (m(b)), basal metabolic rate (BMR), NST, MMR, and minimum thermal conductance (C) on a Chilean fossorial caviomorph (Spalacopus cyanus) from a coastal population, acclimated to cold (15 degrees C) and warm (30 degrees C) conditions. NST was measured as the maximum response of metabolic rate (NST(max)) after injection of norepinephrine (NE) in thermoneutrality minus BMR. Maximum metabolic rate was assessed in animals exposed to enhanced heat-loss atmosphere (He-O2) connected with an open-flow respirometer. Body mass and metabolic variables increased significantly after cold acclimation with respect to warm acclimation but to a low extent (BMR, 26%; NST, 10%; and MMR, 12%). However, aerobic scope (MMR/BMR), calculated shivering thermogenesis (ST), and C did not change with acclimation regime. Our data suggest that physiological plasticity of S. cyanus is relatively low, which is in accordance with a fossorial mode of life. Although little is known about MMR and NST in fossorial mammals, S. cyanus has remarkably high NST; low MMR; and surprisingly, a nil capacity of ST when compared with other rodents.     

Effects of the subterranean herbivorous rodent Spalacopus cyanus on herbaceous vegetation in arid coastal Chile

Summary The impact of the subterranean herbivorous rodent Spalacopus cyanus Molina on the herbaceous vegetation was studied by comparing biomass, species richness and species diversity at the end of the growing season in areas with and without burrows in coastal arid Chile. Total biomass was 60% higher in areas with burrows. This difference was mainly due to the large increase of Mesembryanthemum cristallinum L., a succulent prostrate annual herb. Unexpectedly, bulb biomass of geophytes, eaten by Spalacopus, did not differ between areas. However, in areas with burrows bulbs of geophytes were more numerous and smaller. It is possible that burrowing activities facilitate the occurrence of new small bulbs through seed germination. Species composition and diversity did not differ greatly between areas. Burrowing activities by Spalacopus, the life cycle of Mesembryanthemum, and climate seem to be the most important factors determining species abundance and diversity of herbs in this system.This is a contribution of the Program of Arid Zone Studies of Universidad de La Serena     

A test of the thermal-stress and the cost-of-burrowing hypotheses among populations of the subterranean rodent Spalacopus cyanus

Subterranean mammals show lower than-allometrically expected-basal metabolic rates (BMR), and several competing hypotheses were suggested to explain how physical microenvironmental conditions and underground life affect subterranean mammalian energetics. Two of these are the thermal-stress and the cost-of-burrowing hypotheses. The thermal-stress hypothesis posits that a lower mass-independent BMR reduces overheating in burrows where convective and evaporative heat loss is low, whereas the cost-of-burrowing hypothesis states that a lower mass-independent BMR may compensate for the extremely high energy expenditure of digging during foraging activity. In this paper we tested both hypotheses at an intraspecific level. We compared seven populations of the subterranean rodent Spalacopus cyanus or cururo from different geographic localities with contrasting habitat conditions. We measured BMR and digging metabolic rate (DMR) through open flow respirometry. Our results support neither the thermal-stress nor the cost-of-burrowing hypothesis. Cururos from habitats with contrasting climatic and soil conditions exhibited similar BMR and DMR when measured under similar semi-natural conditions. It is possible that S. cyanus originated in Andean locations where it adapted to relatively hard soils. Later, when populations moved into coastal areas characterized by softer soils, they may have retained the original adaptation without further phenotypic changes.     

Chromosome multiformity in the genus Ctenomys (Rodentia,Octodontidae)

The karotypes of eleven species of the South American burrowing rodents, genus Ctenomys are described, and information on the somatic number of two other species of the same genus is given. The studied species are: C. torquatus (2n =68), C. tuconax (2n =61), C. minutus (2n=50), C. talarum (2n= 48), C. porteousi (2n=48), C. cf. minutus (2n=48), C. australis (2n=46), C. azarae (2n=48), C. latro (2n=42), C. magellanicus fueguinus (2n=36), C. tucumanus (2n=28), C. opimus luteolus (2n=26), and C. occultus (2n =22). This extreme intrageneric variation in somatic number is also reflected by a great amount of diversity in chromosome structure. Karyotypes seem to be rather constant at the species level. Autosomal polymorphism has been found in two of the species, namely C. talarum and C. latro. The hypothesis of the superimposition of Robertsoman rearrangements, pericentric inversions and translocations in the evolution of the karyotype of Ctenomys is advanced. The direction of chromosome change, either toward increase or decrease in chromosome number, is discussed. It is emphasized that high chromosome multiformity is correlated in Ctenomys with a rapid and explosive pattern of species diversification; the meaning of the small size of populations in enhancing the role of chromosome rearrangements in the evolution of Ctenomys is discussed.     

Cytogenetic variation in Ctenomys perrensi (Rodentia, Octodontidae)

A chromosomal study that included the use of uniform stain, G-, C-banding and digestion with restriction enzymes Alu I and Sau 3A was completed in 13 male and two female Ctenomys perrensi collected six localities in Corrientes (NE Argentina). The specimens studied had diploid numbers of 50–57 and FN ranging from 84 to 88. These differences resulted from the presence in heterozygosis or homozygosis of one or two fission products involving chromosomes 1, 2, 4, 7 and 8. In addition, in two localities karyotypes with 2re = 51, 53, 54, 55 and 56 were found, due to the presence of 1–4 C-negative supernumerary chromosomes. All specimens, except for one male and two females, showed more than one different karyotype. Our results suggest that in the localities studied, individuals heterozygous for one or two fission products and/or with a variable number of supernumerary chromosomes are frequently found.     

Molecular cytogenetics and allotetraploidy in the red vizcacha rat, Tympanoctomys barrerae (Rodentia, Octodontidae)

The theoretical impossibility of polyploidy in mammals was overturned by the discovery of tetraploidy in the red vizcacha rat, Tympanoctomys barrerae (2n = 102). As a consequence of genome duplication, remarkably increased cell dimensions are observed in the spermatozoa and in different somatic cell lines of this species. Locus duplication had been previously demonstrated by in situ PCR and Southern blot analysis of single-copy genes. Here, we corroborate duplication of loci in multiple-copy (major rDNAs) and single-copy (Hoxc8) genes by fluorescence in situ hybridization. We also demonstrate that nucleolar dominance, a large-scale epigenetic silencing phenomenon characteristic of allopolyploids, explains the presence of only one Ag-NOR chromosome pair in T. barrerae. Nucleolar dominance, together with the chromosomal heteromorphism detected in the G-banding pattern and synaptonemal complexes of the species' diploid-like meiosis, consistently indicates allotetraploidy. Allotetraploidization can coherently explain the peculiarities of gene silencing, cell dimensions, and karyotypic features of T. barrerae that remain unexplained by assuming diploidy and a large genome size attained by the dispersion of repetitive sequences.     

Olfactory Discrimination of Individual Scents in the Subterranean Rodent Ctenomys talarum (tuco-tuco)

Biological odours that convey cues regarding individual identity can provide valuable information mediating many aspects of mammalian social relationships such us dominance hierarchies, group memberships, territorial and mating activities. The ability of the subterranean rodent, tuco‐tuco (Ctenomys talarum), to discriminate between soiled shavings, urine and faeces from different individuals was investigated using the habituation–discrimination paradigm. Discrimination by both males and females was tested using scents obtained from same‐ and opposite‐sex individuals. Each test subject was habituated for three consecutive days to odour samples from the same individual; on the fourth day a scent from a novel individual was provided. For all odour sources, animals spent significantly less time investigating the habituation scent over successive trials, indicating that animals perceived the stimulus as familiar. For all stimuli, test subjects spent more time investigating the novel odour, rather than the familiar one. Animals spent more time investigating soiled shavings than urine or faeces. Both males and females discriminated novel from familiar odours in shavings and urine regardless of the gender of the odour donors. In contrast, test animals discriminated between familiar and novel odours in feces only when the fecal donors were of different sex from subjects. Possible territorial and reproductive functions of individual scent discrimination are discussed.     

Comparative chromosomal analysis and phylogeny in four Ctenomys species (Rodentia, Octodontidae)

A cytogenetic chromosome study was carried out on specimens of four species of Ctenomys – C. talarum, C. rionegrensis, C. pearsoni and C. dorbignyi –from 10 different populations. The analysis of chromosomes was performed through sequential uniform stain, G and C-banding, and with restriction enzymes. The results obtained are discussed in relation to phylogeny. Chromosome evolution in the species studied suggests that the chromosome number has increased due to fissions, and that a reduction of the amount of constitutive heterochromatin has occurred. Different types of heterochromatin, with different patterns, have been added in parallel during evolution. Some taxonomic suggestions can be deduced from this cytogenetic study.     

Phylogenetic position ofAbalosia and the evolution of the extant Octodontinae (Rodentia, Caviomorpha, Octodontidae)

South American octodontid rodents of the subfamily Octodontinae currently show low species richness but great morphological and chromosomal diversity. This diversity is interpreted alternatively as the remnant of a wider past radiation or as the result of saltational evolution. These hypotheses are discussed in relation to a phylogenetic analysis of the Late Pliocene octodontineAbalosia castellanosi. My results suggest thatAbalosia, together withTympanoctomys andOctomys, is part of a clade of desert specialist propalinal octodontids, which would have differentiated east of the Andes in the emergent semi-deserts of western Argentina. The presence ofAbalosia in the coastal region of central Argentina during the Upper Marplatan Age (Late Pliocene) suggests a pulse of expansion of such arid environments, probably coeval with the global climatic deterioration detected around the transition Gauss-Matuyama magnetic ages. The phylogenetic position ofA. castellanosi suggests that extinction events affected the clade of the octodontine desert specialists. Accordingly, regardless of how rough or gradual the differentiation of the octodontine’s diversity has been, the living representatives seem to be remnants of a wider radiation.     

Spherical bodies in the cytoplasm ofCentaurea cyanus L. (Cornflower) cells

Summary Spherical bodies, 650–750 Å in diameter, are present in undifferentiated callus tissue, and in meristematic and differentiated cells in plants ofCentaurea cyanus L. (Cornflower). Most of these organelles are localised in the cytoplasm immediately external to the nucleus.     

Whole-genome duplications in South American desert rodents (Octodontidae)

The discovery of tetraploidy in the red viscacha rat, Tympanoctomys barrerae (4 n  = 102) has emphasized the evolutionary role of genome duplication in mammals. The tetraploid status of this species is corroborated here by in situ PCR and Southern blot analysis of a single-copy gene. The species meiotic configuration strongly suggests a hybrid derivation. To investigate the origin of T. barrerae further, the recently described Pipanacoctomys aureus was studied. This 92-chromosome species also has a duplicated genome size, redundant gene copy number and diploid-like meiotic pairing, consistent with an event of allotetraploidization. Phylogenetic analysis of mitochondrial sequences indicates sister-group relationships between these two tetraploid rodents. The new karyotypic data and the phylogenetic relationships suggest the participation of the ancestral lineages of Octomys mimax in the genesis of P. aureus . The high overall DNA similarity and shared band homology revealed by genomic Southern hybridization as well as matching chromosome numbers between O. mimax and the descendant tetraploid species support the notion of introgressive hybridization between these taxa.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 443–451.     

Phylogeography and demographic history of the Andean degu,Octodontomys gliroides (Rodentia: Octodontidae)

The Andean degu, Octodontomys gliroides Gervais & d'Orbigny, 1844, has a broad distribution inhabiting pre‐Andean pre‐Puna and Puna environments of tropical South America. In order to understand the phylogeographic patterns of Octodontomys gliroides, we sequenced 579 bp of the mitochondrial DNA control region from 100 individuals collected from 20 populations across its entire distributional range. The phylogenetic and parsimony network, in conjunction with analysis of molecular variance (AMOVA), revealed a structured pattern of geographic differentiation of O. gliroides, with the occurrence of two well‐defined evolutionary lineages: lineage A, restricted to Bolivia and Chile, and lineage B, restricted mainly to Argentina. Analysis of population structure inferred three genetic clusters along the distribution of O. gliroides that mostly agree with the four major barriers inferred by BARRIER analysis (e.g. rivers, salt flats, deserts, and mountain systems). In addition to the significant differentiation found among all levels studied, a positive correlation was identified between genetic and geographic distance, similar to as expected under the isolation‐by‐distance model. The most recent common ancestor of O. gliroides was estimated as c. 5.99 Mya, and the divergence between lineages A and B is estimated to have occurred by the Middle Pleistocene, about 0.69 Mya. The mismatch distributions and neutrality tests suggested a signal of population range expansion for both lineages coincident with major climatic changes that occurred during the wet–dry events of the Pleistocene in the Andean Puna region. Bayesian skyline plots (BSPs) for lineage A suggest a long history of constant population size followed by a period of slight to moderate demographic expansion at c. 0.04 Mya, whereas lineage B remained unclear after BSP analysis, probably because of the limited sample size.     

Cross-species Discrimination of Individual Odors by Hamsters (Muridae: Mesocricetus auratus,Phodopus campbelli)

Golden hamsters, Mesocricetus auratus, and Djungarian hamsters, Phodopus campbelli, Muridae, were tested for the ability to discriminate between individual odors from both their own species and the other species. Hamsters were tested using an habituation technique, in which differences in time spent investigating familiar and novel scents indicate discrimination of individual differences. Both species showed similar patterns of results when tested with flank gland scents from golden hamsters and ventral gland scents from Djungarian hamsters: The duration of investigation of samples from the same indivídual scent donor declined over trials, indicating recognition of this scent, but then increased when a scent from a novel individual was presented, indicating discrimination of individual differences. Thus, the capacity and tendency to respond differentially to signals from different individuals is not confined to a single species, suggesting the lack of species-specificity in the signals and perceptual mechanisms involved in individual recognition by scent. This capacity may be common in mammals, and if so suggests the possibility for considerable knowledge of heterospecific individuals.     

Sequence evolution of the major satellite DNA of the genus Ctenomys (Octodontidae, Rodentia)

Sequence variability of RPCS (repetitive PuvII Ctenomys sequence), the major satellite DNA of octodontid Ctenomys rodents, was analysed in species belonging to three groups of species representing the two patterns of karyotypic evolution in the genus: stable and dynamic karyotypes among closely related species. The studied species represent the overall range of RPCS copy number (2000--6.6x10(6) copies per haploid genome) in the genus. RPCS sequence was characterised by PCR amplification of the genomic consensus sequence and cloned monomers. Our results suggest that RPCS genomic consensus sequence variability correlates with RPCS copy number stability and karyotypic stastis, but not with high or low RPCS copy number values. In contrast, the RPCS gcs shows a mutational profile that is similar across all analysed species. Our data suggest that an RPCS ancestral library of variants was maintained through the cladogenesis of the genus. There is also evidence pointing to the simultaneous contribution of processes of concerted evolution that resulted in a reduced representation of some ancestral variants and their partial replacement for new ones. In addition, analysis of distribution of the variability along the monomer suggests that subsequences of the RPCS are subject to some degree of constraint, probably driven by the recent replicative activity of RPCS in species with high copy number.