Digestive strategies in the South American subterranean rodent Ctenomys talarum

Ctenomys talarum is a subterranean herbivorous rodent which due to its particular life style is frequently exposed to variations in surface environmental conditions (i.e. food quality and availability, temperature). Thus, unlike other subterranean rodents, C. talarum has to buffer both the surface and burrow challenging environmental conditions. We studied the occurrence of digestive strategies at different levels of C. talarum living in their natural habitat. We determined the dimensions of different parts of the gastrointestinal tract and organs along as the activity of key digestive enzymes (disaccharidase, N-aminopeptidase) in different parts of the gut in individuals seasonally caught. The results show that C. talarum exhibits characteristics in the gut at the biochemical level (high disaccharidase activities in small intestine, high N-aminopeptidase activity in the caecum and large intestine, and a seasonal differential modulation of N-aminopeptidase activity in small and large intestines), which could represent adaptive strategies to face seasonal variations in key environmental factors.     

Testing Magnetic Orientation in a Solitary Subterranean Rodent Ctenomys talarum (Rodentia: Octodontidae)

To test for the hypothesis that Ctenomys talarum can use the earth's magnetic field for spatial orientation, we carried out field and laboratory experiments to analyse if C. talarum burrows present any geomagnetic orientation in their natural habitat, if C. talarum show any spontaneous directional preference when starting to excavate their burrows and if this subterranean rodent is capable to use the earth's magnetic field to orient towards a goal in a complex maze. No correlation between the burrowing direction and the earth's magnetic field was found. We could not find any evidence for any spontaneous directional preference when starting to excavate the burrows in C. talarum. The change of the horizontal vector of the geomagnetic field did not affect the ability of this rodent to orient towards a goal in an artificial labyrinth. Explanations for these results and other possible mechanisms of orientation that could be used by C. talarum are discussed.     

Use of vegetation chemical signals for digging orientation in the subterranean rodent Ctenomys talarum (Rodentia: Ctenomyidae)

Sensory modalities involved in the localization and selection of food represent critical information for understanding the foraging behavior of subterranean rodents. The objective of this study was to determine if a subterranean rodent that forages on aboveground plant parts, Ctenomys talarum, is able to detect the presence of odorous chemicals released by the plants into the soil to guide its excavation, as has been shown for subterranean species that forage on roots and bulbs. Individuals were introduced into an artificial Y‐maze, whose arms were filled with sandy soil in which plants either had or had not been growing (control). Digging activity exhibited in each soil type was recorded. The following plant species, present in the natural habitat of C. talarum, were used: Panicum racemosum (three different concentrations), Cortadeira sp., Margiricarpus pignatus, Ambrosia sp. and Raphanus sativus. The individuals allocated more time to excavation in the soil in which vegetation had been growing in comparison with the control for the five analysed plant species, except in the case of P. racemosum at its lowest concentration. The number of individuals that completed excavation in the tube‐containing soil in which plants had been growing was significantly higher than in the tube‐containing soil in which no plants had been growing, with the exception of P. racemosum at its lowest concentration and R. sativus. The results of the present study suggest that C. talarum have the ability to use olfaction to orient their digging while foraging even though members of this species consume mainly aboveground plant parts.     

A method for studying social and reproductive behaviour of subterranean rodents in captivity

A methodology for studying the social and reproductive behaviour of solitary subterranean rodents under laboratory conditions is proposed. A first account ofCtenomys talarum (Thomas, 1898) behaviour is also provided with the aim of evaluating the proposed methodology and to advance presently unknown information on its social behaviour and mating system. The device is a seminatural enclosure, departing from traditional test cages with respect to increased: (1) size, (2) structural complexity, (3) social complexity, and (4) resemblance to natural conditions. It consists of artificial burrows each comprising 3.5 m of tunnel, a resource cage and a nest box, resembling the structural complexity described forC. talarum burrows. Burrows are connected to a common space, which allows social interaction among various individuals. Animals were observed in the seminatural enclosure — 3 females and 2 males, in accordance with sex ratios found in natural populations — for a period of 6 months. We obtained data related to reproductive and social behaviour: marking, aggression, vocalization, courtship and copulation, pregnancy, pup development, and parental care. The proposed system enables the collection of behavioural data as yet unavailable due to the secretive habits and aggressiveness that characterize this group of rodents, coupled with the difficulties associated with simulating subterranean conditions.     

Juvenile vocalizations ofCtenomys talarum (Rodentia: Octodontidae)

We analysed the physical structure and functional interpretation of juvenile vocalizations ofCtenomys talarum Thomas, 1898. Two sounds, one true vocalization (care-elicitation call) and one mechanical sound (nursing sound) were recorded during the nestling period. Care-elicitation calls were emitted by isolated pups and caused the mother to respond by immediately approaching the pups to take care of them. This maternal response to the care-elicitation calls ofC. talarum pups, together with the production of these vocalizations during the first weeks after birth, when pups depend exclusively on their mother to obtain food and maintain their body temperature, give preliminary support for the recent theory that care-elicitation cries are honest advertisements of offspring need.     

Postnatal ontogeny of limb proportions and functional indices in the subterranean rodent Ctenomys talarum (Rodentia: Ctenomyidae)

Burrow construction in the subterranean Ctenomys talarum (Rodentia: Ctenomyidae) primarily occurs by scratch‐digging. In this study, we compared the limbs of an ontogenetic series of C. talarum to identify variation in bony elements related to fossorial habits using a morphometrical and biomechanical approach. Diameters and functional lengths of long bones were measured and 10 functional indices were constructed. We found that limb proportions of C. talarum undergo significant changes throughout postnatal ontogeny, and no significant differences between sexes were observed. Five of six forelimb indices and two of four hindlimb indices showed differences between ages. According to discriminant analysis, the indices that contributed most to discrimination among age groups were robustness of the humerus and ulna, relative epicondylar width, crural and brachial indices, and index of fossorial ability (IFA). Particularly, pups could be differentiated from juveniles and adults by more robust humeri and ulnae, wider epicondyles, longer middle limb elements, and a proportionally shorter olecranon. Greater robustness indicated a possible compensation for lower bone stiffness while wider epicondyles may be associated to improved effective forces in those muscles that originate onto them, compensating the lower muscular development. The gradual increase in the IFA suggested a gradual enhancement in the scratch‐digging performance due to an improvement in the mechanical advantage of forearm extensors. Middle limb indices were higher in pups than in juveniles–adults, reflecting relatively more gracile limbs in their middle segments, which is in accordance with their incipient fossorial ability. In sum, our results show that in C. talarum some scratch‐digging adaptations are already present during early postnatal ontogeny, which suggests that they are prenatally shaped, and other traits develop progressively. The role of early digging behavior as a factor influencing on morphology development is discussed. J. Morphol. 275:902–913, 2014. © 2014 Wiley Periodicals, Inc.     

Subterranean rodents of the genus Ctenomys (Caviomorpha, Ctenomyidae) follow the converse to Bergmann's rule

Aim We analysed body‐size variation in relation to latitude, longitude, elevation and environmental variables in Ctenomys (tuco‐tucos), subterranean rodents in the Ctenomyidae (Caviomorpha). We tested the existence of inter‐ and intraspecific size clines to determine if these rodents follow Bergmann's rule, to compare intra‐ and interspecific size trends and to assess the relevance of the subterranean lifestyle on these trends. Location South America, south of 15° latitude. Methods This paper is based on 719 specimens of tuco‐tucos from 133 localities of Argentina, Bolivia, Chile, Paraguay, Peru and Uruguay, representing 47 named species and 32 undescribed forms. Intraspecific analyses were performed for Ctenomys talarum Thomas, 1898 and the Ctenomys perrensi Thomas, 1896 species complex. Head and body length and weight were used for estimating body size. Geographical independent variables included latitude, longitude and altitude. Environmental independent variables were mean minimal and maximal monthly temperature, mean annual temperature, mean minimal and maximal precipitation, and total annual precipitation. To estimate seasonality, the annual variability of the climatic factors was calculated as their coefficients of variation and the difference between maximum and minimum values. Mean annual actual evapotranspiration (AET), and mean annual, January (summer) and July (winter) potential evapotranspiration (PET) values were also calculated for each locality, as well as annual, summer and winter water balance (WB). Statistical analyses consisted of simple and multiple regression and nonparametric correlation. Results Body size of Ctenomys decreases interspecifically from 15°00′ S to 48°15′ S and from 56°33′ W to 71°46′ W, and is positively correlated with ambient temperature and precipitation. The best predictors of body size according to multiple regression analyses were mean annual temperature, the difference between mean maximum and minimum annual temperatures, annual PET, the difference between summer and winter PET, and annual and winter water balance. These patterns are repeated, but not identically, at a smaller geographical scale within the species C. talarum and the superspecies C. perrensi. Main conclusions Tuco‐tucos follow the converse to Bergmann's rule at the interspecific level. At the intraspecific level some parallel trends were observed, but the smaller scale of these analyses, involving a very reduced variation of environmental factors, necessitates caution in interpreting results. The subterranean lifestyle probably insulates these rodents from the external temperature. The observed latitudinal body‐size gradients are more probably related to seasonality, ambient energy, primary productivity and/or intensity of predation.     

Source Odor,Intensity, and Exposure Pattern Affect Antipredatory Responses in the Subterranean Rodent Ctenomys talarum

Predation is a strong selective force, and prey species may show specific adaptations that allow recognition, avoidance, and defense against predators. Facing a situation of predatory risk, anxiety constitutes a reaction of adaptive value, allowing to evaluate the potential risk of this encounter as well as to generate a physiological and behavioral response. Previous studies in the subterranean rodent Ctenomys talarum revealed that exposure to predator odors (urine or fur) generates an anxiety state and induces behavioral changes. However, no differences between the responses generated by both odor sources were observed, although fur odors may indicate a higher level of predatory immanence. Therefore, the aim of this study was to evaluate the behavioral and physiological responses of C. talarum to different intensities of predator odors (urine and fur) and to the repeated exposition to the same odorous stimulus. When comparing the highest behavioral effects elicited by both predatory odors on C. talarum, our study supports the assumption that fur odors are more anxiogenic than urine, while the former provoked significant changes in the distance traveled, the number of arm entries and time in transparent arms in the elevated plus maze; cat urine only caused slight changes on those behavioral parameters. Furthermore, we also found that the intensity of natural predator odor presented to tuco‐tucos has a role on the appearance of defensive behaviors, although an amount‐dependent relationship between predator odor and anxiety levels was not observed. Finally, while individuals exposed for 1 day to fur odor displayed an evident anxiety state, those exposed repeatedly for 5 consecutive days did not differ with the control group in their behavioral response, indicating a clear habituation to the predatory cue. In our intensity and habituation experiments, we did not find differences in the measured physiological parameters among control individuals, exposed to different cues intensity (urine and fur odor) and exposed only once or for 5 days to fur odor. These results provide valuable evidence that the types of predatory odor, along with the frequency of exposition, are important determinants of the appearance, strength, and extinction of defensive behaviors in the subterranean rodent C. talarum.     

Effects of contrasting demographic histories on selection at major histocompatibility complex loci in two sympatric species of tuco‐tucos (Rodentia: Ctenomyidae)

To explore the impact of history on selection and genetic structure at functional loci, we compared patterns of major histocompatibility complex (MHC) variability in two sympatric species of ctenomyid rodents with different demographic backgrounds. Although Ctenomys talarum has experienced a stable demographic history, Ctenomys australis has undergone a recent demographic expansion. Accordingly, we predicted that MHC allele frequency distributions should be more skewed, differences between coding and noncoding regions should be less pronounced, and evidence of current selection on MHC loci should be reduced in C. australis relative to C. talarum. To test these predictions, we compared variation at the MHC class II DRB and DQA genes with that at multiple neutral markers, including DQA intron 2, the mitochondrial control region, and 8–12 microsatellite loci. These analyses supported the first two of our predictions but indicated that estimates of selection (based on ω‐values) were greater for C. australis. Further exploration of these data, however, revealed differences in the time frames over which selection appears to have acted on each species, with evidence of contemporary selection on MHC loci being limited to C. talarum. Collectively, these findings indicate that demographic history can substantially influence genetic structure at functional loci and that the effects of history on selection may be temporally complex and dynamic. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 260–277.     

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. Accepted: 16 September 1996     

Vocal repertoire of the social Mashona mole-rat (Fukomys darlingi) and how it compares with other mole-rats

Vocalizations play a major role in communication of mammals with subterranean lifestyles since other senses are dramatically restricted in the environment of below ground burrows. In our study, we recorded vocalizations of 10 adult males and 10 adult females of a social bathyergid, the Mashona mole-rat (Fukomys darlingi) in different behavioural contexts. Vocalizations were divided into four categories according to behavioural contexts. Similar to other subterranean mammals, the range of Mashona mole-rat calls is shifted towards lower frequencies. We described 10 types of true vocal signals and 2 mechanical sounds. The vocal repertoire of the Mashona mole-rat is less rich compared to other social mole-rats, corresponding with its low mean family size. Interestingly, this species has a higher diversity in contact and distress calls, while using a relatively low number of aggressive signals.     

Female preference for males that have exclusively marked or invaded territories depends on male presence and its identity in the subterranean rodent Ctenomys talarum

Territorial scent‐marking provides chemical records of male competitive interactions that are available to females, who gain valuable information to assess and identify best quality partners. In this context, the solitary subterranean rodent tuco‐tuco (Ctenomys talarum) offers excellent possibilities to evaluate the effects of male exclusive scent‐marking of territories on female assessment. For evaluation, we used wild caught individuals of C. talarum, manipulated their scent marks within the territories in captive conditions and staged preference tests where females were able to choose between exclusive and invaded territories. The evaluation was performed in two scenarios considering the identity of the intruder scent mark: territories invaded by a strange male and territories invaded by a neighbour male. Females investigated the chemical cues deposited on the substrate of the exclusively marked territory more frequently. Next, females displayed equal interest to scent samples of both males presented in a Y‐maze. Finally, when females could gain access to both individually isolated males and their scent‐marked territories, they spent more time within invaded territories despite they visited them with the same frequency. Moreover, females tried to get in contact by scratching the mesh of the owner of the invaded territory more frequently. We found that females of C. talarum evaluate the homogeneity (exclusiveness) of scent marks within a male territory and then show preferences in relation to the identity of the intruder's scent –whether strange or neighbour.     

Comparative respiratory strategies of subterranean and fossorial octodontid rodents to cope with hypoxic and hypercapnic atmospheres

Subterranean rodents construct large and complex burrows and spend most of their lives underground, while fossorial species construct simpler burrows and are more active above ground. An important constraint faced by subterranean mammals is the chronic hypoxia and hypercapnia of the burrow atmosphere. The traits, regarded as “adaptations of rodents to hypoxia and hypercapnia”, have been evaluated in only a few subterranean species. In addition, well-studied subterranean taxa are very divergent to their sister groups, making it difficult to assess the adaptive path leading to subterranean life. The closely related sister genera Octodon and Spalacopus of Neotropical rodents offer a unique opportunity to trace the evolution of physiological mechanisms. We studied the ventilatory responses of selected octodontid rodents to selective pressures imposed by the subterranean niche under the working hypothesis that life underground, in hypoxic and hypercapnic conditions, promotes convergent physiological changes. To perform this study we used the following species: Spalacopus cyanus (the subterranean coruros) and Octodon degus (the fossorial degus) from central Chile. Ventilatory tidal volume and respiratory frequency were measured in non-anaesthetized spontaneously breathing animals. Acute hypoxic challenges (O₂ 1–15%) and hypercapnia (CO₂ 10%) were induced to study respiratory strategies using non-invasive whole body pletismography techniques. Our results show that coruros have a larger ventilatory response to acute hypoxia as than degus. On the other hand, hypercapnic respiratory responses in coruros seem to be attenuated when compared to those in degus. Our results suggest that coruros and degus have different respiratory strategies to survive in the hypoxic and hypercapnic atmospheres present in their burrows.     

Ontogenetic integration between force production and force reception: a case study in Ctenomys (Rodentia: Caviomorpha)

During ontogeny, complex adaptations undergo changes that sometimes entail different functional capabilities. This fact constrains the behaviour of organisms at each developmental stage. Rodents have ever‐growing incisors for gnawing, and a powerful jaw musculature. The incisors are long enough, relative to their diameter, to be affected by bending stresses. This is particularly true in the subterranean Ctenomys that uses its incisors for digging. We measured bite force (BF) in individuals of different ages using a force transducer. We estimated incisor section modulus Z, a geometrical parameter proportional to bending strength. A relative strength indicator was calculated as S = Z/BF incisor length. We found that ontogenetic BF scales to body mass with positive allometry. However, an anova showed non‐significant differences in S, neither between sexes nor among age classes. This result implies that during growth, incisors might have a rather similar ability to withstand bending stresses from increasing masticatory forces, what may be considered evidence of ontogenetic integration of force production (by muscles) and force reception (by the incisors). This fact well correlates with the observation that pups and juveniles of C. talarum incorporate solid foods shortly after birth, and they are able to dig burrows early in life.     

Tuco-tucos’ vocalization output varies seasonally (<Emphasis Type="Italic">Ctenomys pearsoni</Emphasis>; Rodentia,Ctenomyidae): implications for reproductive signaling

Tuco-tucos are subterranean rodents endemic of South America. Ctenomys pearsoni is a solitary species from southwestern Uruguay. Each individual occupies its own burrow and aggressively defends it, except for juveniles before dispersing and couples during reproduction. We tried to understand how these animals find a partner and how they know their reproductive state, avoiding to spend excess energy burrowing to locate those partners for reproduction and avoiding above-ground predation. We studied a C. pearsoni population in the field from June 2005 until March 2007, using individually identified animals, some fitted with radio-tracking collars. For their long-range vocalizations, we recorded the number of vocalizations, number of series (groups of notes composing the vocalization) emitted, time of day of the emission, and emitter identity. Samples were taken by listening to the emissions. Results show that the number of emissions changes along the year, being higher during the reproductive season. Males emit more frequently than females and do it throughout the year. Female vocalizations rise in number when reproduction starts and then decline in number through pregnancy and/or until juveniles disperse and also vary in length being longer during the beginning of the breeding period. These results suggest that female vocalization (i.e., repetition and duration) would inform about emitter’s location, sex, and reproductive condition.     

Sound transmission and burrow characteristics of the subterranean rodentCtenomys talarum (Rodentia: Ctenomyidae)

Males of tuco-tucoCtenomys talarum Thomas, 1898 use particular burrow’s entrances to emit their territorial vocalization. Therefore we studied the internal structure of these entrances and the possible effect on the emission and propagation of airborne sounds. Externally, the burrow entrances used by tuco-tucos males to vocalize were characterized by the absence of sand mounds around their openings. Internally, most of the burrow’s entrances consisted of a main, relatively straight, tunnel of 30–40 cm length, with a diameter of 5.7–6.4 cm. After passing through the burrow’s entrance, the low-frequency components of an artificial signal played back inside the tunnel were not only less attenuated but also amplified (measured at 10–30 cm from the burrow opening). Therefore, the emission of territorial vocalizations inside the particular burrow’s entrances may be considered as a complex adaptative behavior, in which burrow structure improves the signal emission and propagation. Moreover, this work also showed thatC. talarum’s territorial vocalization seems to be adequate for long, inter-burrow communication, since its physical characteristics (high amplitude and low main frequency) are concomitant with the frequencies that are better transmitted in the natural habitat of this species of subterranean rodent.     

Chromosomal polymorphism and small karyotypic differentiation in a group of Ctenomys species from Central Argentina (Rodentia: Octodontidae)

Cytogenetic analysis was performed in six nominal taxa of the genus Ctenomys with a diploid number of 2n=47/48. The studied species were: C. australis (2n=48, FN=76); C. mendocinus (2n=47/48, FN=68/75/76); C. porteousi (2n=47/48, FN=71/72/73); C. azarae (2n=47, FN=71); C. sp. (chasiquensis) (2n=47/48); and C. talarum (2n=48, FN=80). The first three species shared the whole complement, C. talarum shares with them 19 arms from a total of 43 (44%). In all species analyzed constitutive heterochromatin was detected in most short arms, and in several centromeres. Polymorphisms for several pairs involving the heterochromatic short arms together with a complex polymorphism of pair A1 were found in C. azarae, C. sp., C. mendocinus and C. porteousi. Intraindividual variation found in one specimen of C. porteousi involving heterochromatic arms is discussed.These results lead us to propose the inclusion of all species except C. talarum, within a complex called the mendocinus-group. A new case of conservatism for chromosomal number in the genus Ctenomys is found in this group.     

Hearing in coruros (<Emphasis Type="Italic">Spalacopus cyanus</Emphasis>): special audiogram features of a subterranean rodent

Learning curves and behavioural audiograms of subterranean, socially living coruros (Spalacopus cyanus) were obtained using a positive reinforcement conditioning procedure. The individually varying audiograms revealed best hearing at frequencies between 1.25 and 1.6 kHz, which corresponds with the common pattern established in subterranean rodents studied so far. However, the broad hearing range covering frequencies at least between 0.25 and 20 kHz coupled with the high sensitivity (average minimum 7 dB) that is found in coruros are atypical features for audiograms of subterranean rodents, which usually show restricted high-frequency hearing ranges and very poor sensitivity. Hearing at low frequencies (peaks at frequencies <1 kHz), which may be related to sound transmission in underground burrows, and high sensitivity at 1.25/1.6 kHz are discussed in relation to vocalization. In addition to these peaks, a third peak at 8 kHz—probably a plesiomorphic feature of mammals—may be of significance in aboveground communication.     

Heterogeneity of heterochromatin in six species ofCtenomys (Rodentia: Octodontoidea: Ctenomyidae) from Argentina revealed by a combined analysis of C- and RE-banding

Exceptional chromosomal variability makesCtenomys an excellent model for evolutionary cytogenetic analysis. Six species belonging to three evolutionary lineages were studied by means of restriction endonuclease and C-chromosome banding. The resulting banding patterns were used for comparative analysis of heterochromatin distribution on chromosomes. This combined analysis allowed intra- and inter-specific heterochromatin variability to be detected, groups of species belonging to different lineages to be characterized, and phylogenetic relationships hypothesized from other data to be supported. The “ancestral group”,Ctenomys pundti andC. talarum, share three types of heterochromatin, the most abundant of which was also found in C. aff.C. opimus, suggesting that the latter species also belongs to the “ancestral group”. Additionally, within the subspeciesC. t. talarum, putative chromosomal rearrangements distinguishing two of the three chromosomal races were identified. Two species belong to an “eastern lineage”,C. osvaldoreigi andC. rosendopascuali, and share only one type of heterochromatin homogeneously distributed across their karyotypes.C. latro, the only analyzed species from the “chacoan” lineage, showed three types of heterochromatin, one of them being that which characterizes the “eastern lineage”.C. aff.C. opimus, because of its low heterochromatin content, is the most primitive karyotype of the genus yet described. The heterochromatin variability showed by these species, reflecting the evolutionary divergence toward different heterochromatin types, may have diverged since the origin of the genus. Heterochromatin amplification is proposed as a trend withinCtenomys, occurring independently of chromosomal change in diploid numbers.     

Energetics and thermoregulation during digging in the rodent tuco-tuco (Ctenomys talarum)

For subterranean rodents, searching for food by extension of the tunnel system and maintenance of body temperature are two of the most important factors affecting their life underground. In this study we assess the effect of ambient temperature on energetics and thermoregulation during digging in Ctenomys talarum. We measured V˙o₂ during digging and resting at ambient temperature (T_a) below, within, and above thermoneutrality. Digging metabolic rate was lowest at T_a within the thermoneutral zone and increased at both lower and higher temperatures, but body temperature (T_b) remained constant at all T_as. Below thermoneutrality, the cost of digging and thermoregulation are additive. Heat production for thermoregulation would be compensated by heat produced as a by-product of muscular activity during digging. Above thermoneutrality, conduction would be an important mechanism to maintain a constant T_b during digging.