Nutritional responses to different diet quality in the subterranean rodent Ctenomys talarum (tuco-tucos)

Nutritional response to different diet quality was examined in the subterranean rodent Ctenomys talarum (tuco-tuco). Animals maintained in captive conditions were fed with three plant species that differed in their fibre content. Tuco-tucos showed the ability to perform adjusts in short time lapse in response to diet quality; food ingestion, egestion and feces ingestion changed in animals under different plant species diets. Time budget, mainly time devoted to feeding and activity accompanied such changes. Coprophagy was practiced along the day and night following the arrhythmic activity pattern found for this species. Feces reingestion was not associated to resting. Furthermore, it was observed during fresh food ingestion, being pellets chewed. Soft and hard feces differed in morphological and nutritional characteristics.     

Acoustic signals of a solitary subterranean rodent Ctenomys talarum (Rodentia: Ctenomyidae): physical characteristics and behavioural correlates

The purpose of this study was to analyse and describe vocalizations of a solitary subterranean rodent, Ctenomys talarum. In adult C. talarum five different sounds (four true vocalizations and one mechanical sound) were recorded during different behavioural contexts. Using data from the laboratory and literature, we classified these vocalizations as territorial, distress, and mating calls. We found that the vocalization range in C. talarum is shifted towards low frequencies, which transmit better in underground burrows and match well the hearing range described for other species of subterranean rodents. These low-frequency vocalizations, also found in other non-related subterranean rodents, may reflect an adaptation to the acoustic conditions of the habitat. Electronic Publication     

DNA fingerprinting reveals polygyny in the subterranean rodent Ctenomys talarum

DNA fingerprinting was used to characterize patterns of paternity in two populations of Ctenomys talarum from Buenos Aires Province, Argentina. The multilocus probe PV47-2 was used to detect variation in genomic DNA extracted from 12 females, their 32 offspring, and 14 putative sires. For 11 out of 12 litters examined, a single male capable of providing all nonmaternal bands was identified. Within each study population, individual males sired more than one litter, suggesting that C. talarum is polygynous. No evidence of multiple paternity of litters was found. High band-sharing values among females suggest that further research is needed to assess the population genetic structure of this species.     

Maximal thermogenic capacity and non-shivering thermogenesis in the South American subterranean rodent Ctenomys talarum

Subterranean rodents inhabit closed tunnel systems that are hypoxic and hypercapnic and buffer aboveground ambient temperature. In contrast to other strictly subterranean rodents, Ctenomys talarum exhibits activity on the surface during foraging and dispersion and hence, is exposed also to the aboveground environment. In this context, this species is a valuable model to explore how the interplay between underground and aboveground use affects the relationship among basal metabolic rate (BMR), cold-induced maximum metabolic rate (MMR), shivering (ST), and non-shivering thermogenesis (NST). In this work, we provide the first evidence of the presence of NST, including the expression of uncoupling proteins in brown adipose tissue (BAT), and shivering thermogenesis in Ctenomys talarum, a species belonging to the most numerous subterranean genus, endemic to South America. Our results show no differences in BMR, cold-induced MMR, and NST between cold- (15?°C) and warm- (25?°C) acclimated individuals. Furthermore, thermal acclimation had no effect on the expression of mitochondrial uncoupling protein 1 (UCP1) in BAT. Only cytochrome c oxidase (COX) content and activity increased during cold acclimation. When interscapular BAT was removed, NST decreased more than 30?%, whereas cold-induced MMR remained unchanged. All together, these data suggest that cold-induced MMR reaches a maximum in warm-acclimated individuals and so a probable ceiling in NST and UCP1 expression in BAT. Possible thermogenic mechanisms explaining the increase in the oxidative capacity, mediated by COX in BAT of cold-acclimated individuals and the role of ST in subterranean life habits are proposed.     

Phenotypic flexibility of digestive morphology and physiology of the South American omnivorous rodent Akodon azarae (Rodentia: Sigmodontinae)

We have determined the occurrence of responses at different levels (morphological, physiological and biochemical) in the omnivorous rodent Akodon azarae upon cold acclimation (15 degrees C). A short-term enhancement in food consumption appeared to account for the maintenance of both mass and body composition. At the morphological level, the main response was an increase in the dimensions of small intestine, which constitutes the section of the gut where absorption and secretion take place. An increase in sucrase specific activity was only found in small intestine. Sucrose independent maltase activity was very low since 99.8% of total maltase activity was due to sucrase-isomaltase (SI) complex. Protease specific activities were not affected. The fact that resting metabolic rates determined at 15 and 23 degrees C were similar in cold acclimated animals suggests a change in lower critical temperature. In conclusion, our results show that A. azarae exhibits different strategies to support cold environment that could lead to an enhancement in digestion and absorption efficiency. Furthermore, this work suggests that low temperature is an independent cue of other environmental factors to trigger the strategies allowing the maintenance of body condition in A. azarae.     

Reactions to disturbances in the context of antipredatory behaviour in a solitary subterranean rodent

We investigated reactions of free-living silvery mole-rats (Heliophobius argenteocinereus) to anthropogenic disturbances. Mole-rats detected soil vibrations caused by man carefully walking at a distance of up to 6 m (proved by radio-telemetry). Occasionally, mole-rats encountered outside a nest retreated there after this type of disturbance. After having their burrows broken into, the mole-rats retreated into deep tunnels, separating themselves from the rest of the burrows by soil plugs. Trapping success of silvery mole-rats using live traps for subterranean rodents was low, which contrasts with data so far published on social bathyergids. Antipredatory function of examined behaviours is discussed.     

Phylogeographical structure in the subterranean tuco-tuco Ctenomys talarum (Rodentia: Ctenomyidae): contrasting the demographic consequences of regional and habitat-specific histories

In this work we examined the phylogeography of the South American subterranean herbivorous rodent Ctenomys talarum (Talas tuco-tuco) using mitochondrial DNA (mtDNA) control region (D-loop) sequences, and we assessed the geographical genetic structure of this species in comparison with that of subterranean Ctenomys australis, which we have shown previously to be parapatric to C. talarum and to also live in a coastal sand dune habitat. A significant apportionment of the genetic variance among regional groups indicated that putative geographical barriers, such as rivers, substantially affected the pattern of genetic structure in C. talarum. Furthermore, genetic differentiation is consistent with a simple model of isolation by distance, possibly evidencing equilibrium between gene flow and local genetic drift. In contrast, C. australis showed limited hierarchical partitioning of genetic variation and departed from an isolation-by-distance pattern. Mismatch distributions and tests of neutrality suggest contrasting histories of these two species: C. talarum appears to be characterized by demographic stability and no significant departures from neutrality, whereas C. australis has undergone a recent demographic expansion and/or departures from strict neutrality in its mtDNA.     

Energy and distribution in subterranean rodents: sympatry between two species of the genus Ctenomys

The low basal metabolic rate (BMR) observed in subterranean rodents, compared to that of surface-dwelling species of comparable size, has been proposed to be an adaptation to underground life. Two main hypotheses have been proposed to explain this finding, the cost of burrowing and the thermal stress. The former states that the low BMR is due to the high cost of extending the tunnel system whereas the other relates it to the possibility of overheating in burrows where evaporative and convective heat exchange are restricted. Additionally, both hypotheses related the energetics of subterranean rodent with spatial distribution. The genus Ctenomys is an excellent model to evaluate the cost of burrowing or thermal stress, since they are widely distributed, with members differing markedly in body mass. The aim of this study was to assess digging and basal energetics in two Ctenomys species that live in sympatry in a coastal grassland, but differ in their microspatial distribution by soil preference. We used the obtained energetic data to test both energy-distribution hypotheses. We measured BMR and digging metabolic rate (DMR) through open flow respirometry in two species exposed to soft and hard soils. In brief, DMR in Ctenomys talarum (100-170 g), as in Ctenomys australis (250-600 g), was unaffected by soil hardness. Within thermoneutral zone of each species, DMR/RMR quotient was lower in the smaller species. Our data did not support the thermal stress hypothesis, but the cost of burrowing hypothesis was not rejected. Other alternative hypotheses are proposed to explain the distribution of C. talarum and C. australis.     

Predation upon the subterranean rodent Ctenomys talarum (tuco-tucos) by Buteo polyosoma (red-backed hawks) in coastal grasslands of Argentina

Differential predation upon tuco-tucos (Ctenomys talarum) by red-backed hawks (Buteo polyosoma) is reported, considering the characteristics that could lead to prey vulnerability and to predator selectivity. Predation was evaluated through analysis of 100 pellets and 20 prey remains collected in coastal grasslands at Mar de Cobo (Buenos Aires, Argentina) during winter (May to August) 2003–2004. The tuco-tucos represented the main component in the diet of red-backed hawks, registering a high consumption of sub-adult individuals (49.3%). Juvenile individuals (42.0%) were overrepresented and adults (8.7%) were underrepresented in relation to their field frequencies (14.4 and 43.1%, respectively), whereas sub-adults did not show significant differences. This high consumption of smaller tuco-tucos would be based on the higher vulnerability of young individuals to predation rather than raptor's handling constraints on bigger individuals. Our results indicate that a strong predator–prey relationship between tuco-tucos and red-backed hawks is established at the study area, and that tuco-tucos represent a key component for the survival of wintering hawks.

Reportamos la depredación diferencial sobre el tuco-tuco (Ctenomys talarum) por el aguilucho común (Buteo polyosoma), considerando las características que podrían determinar la vulnerabilidad de la presa y la selectividad del predador. La depredación fue evaluada mediante el análisis de 100 egagrópilas y 20 restos presa recolectados en pastizales costeros de la localidad de Mar de Cobo (Buenos Aires, Argentina) durante el periodo invernal Mayo–Agosto de 2003–2004. El tuco-tuco representó el principal componente en la dieta del aguilucho común, registrándose un alto consumo de individuos subadultos (49.3%). Los individuos juveniles (42.0%) fueron sobrerrepresentados y los adultos (8.7%) fueron subrepresentados en la dieta en relación a sus frecuencias en el campo (14.4 y 43.1%, respectivamente), mientras que los subadultos no mostraron diferencias significativas. Este elevado consumo de individuos más pequeños radicaría en una mayor vulnerabilidad a la depredación de los juveniles más que en restricciones de manipuleo del predador sobre las presas más grandes. Nuestros resultados indican que existe una estrecha relación predador–presa entre el tuco-tuco y el aguilucho común, y que los tuco-tucos representan un componente clave para la supervivencia invernal de los aguiluchos.     

Population and species boundaries in the South American subterranean rodent Ctenomys in a dynamic environment

Subterranean rodents of the genus Ctenomys are an interesting system to assess the effects of habitat instability on the genetic structure of populations. The perrensi group is a complex of three species (C. roigi, C. perrensi and C. dorbignyi) and several forms of uncertain taxonomic status, distributed in the vicinity of the Iberá wetland in Argentina. Because of limited availability of suitable dry habitat, Ctenomys populations are distributed patchily around a vast mosaic of marshes, swamps and lagoons and become connected or isolated over time, depending particularly on the precipitation regime. Genetic variation at 16 microsatellite loci in 169 individuals collected in the area revealed eight clusters of populations which are thought to be evolutionary units, but which do not fit previous species limits. We interpret this lack of congruence between taxonomy and genetic structure as the result of a dynamic population structure. Where populations become connected, hybridization is possible. Where populations become isolated, rapid genetic divergence may occur. In the perrensi group, it appears that both of these factors disrupt the association between different genetic and morphological characters. The study of multiple characters is crucial to the understanding of the recent evolutionary history for dynamic systems such as this. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 368–383.     

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.     

Foraging strategy in a subterranean rodent,Spalax ehrenbergi: a test case for optimal foraging theory

Summary The foraging behavior of the subterranean mole rat Spalax ehrenbergi (Rodentia, Spalacidae) was tested according to the framework of optimal foraging theory. We compared the frequencies of food species hoarded in storage chambers of mole rats with the frequencies of these species occurring in the vicinity of the mole rats' nest mounds during the winter and spring seasons. In addition, we examined the food composition of several summer nest mounds. Laboratory observations were conducted in order to test the foraging behavior of mole rats under simulated subterranean conditions. The mole rat is a generalist and collects a variety of food species. Out of 33 plant species that were hoarded by mole rats in the 21 studied nest mounds, 61% (n=20) were geophytes, 21% (n=7) perennial herbs, 15% (n=5) annual herbs and 3% (n=1) dwarf shrubs. The frequency of each collected species in the 16 winter and spring nest mounds is in general accordance with its frequency in the mole rat's territory. This implies that the mole rat randomly samples the food reserve of its territory without special preference or directed search for a particular species. The collection or avoidance of any food item is not dependent on the presence or absence of any other food item. We suggest that the foragin generalism of the mole rat is a product of the constraints of a subterranean niche — the necessity to hoard food as much as possible in a limited time period and the high energetic investment of tunneling to the food items.     

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     

Inter and intra-specific hybridization in tuco-tucos (Ctenomys) from Brazilian coastal plains (Rodentia: Ctenomyidae)

The present work describes chromosomal polymorphisms in zones of contact between divergent populations of Ctenomys minutus parapatrically distributed in the coastal plain of southern Brazil, and inter-specific hybridization with C. lami a closely related species. A sample of 171 specimens from 32 sample sites distributed along 161 km of the coastal plain was cytogenetically analyzed. Nine polymorphic populations were found: four with specimens with 2n = 46–48 (autosomal arm number (AN) = 76); three only have specimens with 2n = 47 and 48; one population sampled presented specimens with 2n = 43–46 (AN = 74–76) and one population with 2n = 50–52 (AN = 76–80). The remainder populations were fixed for 2n = 42, 46 or 48. The variation is the result of Robertsonian mechanisms of chromosomal evolution and a fusion in tandem rearrangement. The polymorphisms have been considered the result of secondary contact of populations after divergence in allopatry. The geomorphological evolution of the coastal plain provides clues to the possible existence of past geographic barriers acting over populations of Ctenomys, during the Holocene.     

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.     

Graphidioides subterraneus n. sp. (Nematoda: Trichostrongyloidea) from the South American subterranean rodent Ctenomys talarum Thomas, 1898 (Rodentia: Octodontidae)

A new nematode species, Graphidioides subterraneus n. sp., found in the stomach of C. talarum from Argentina is described. The new species more closely resembles G. mazzai Lent & Freitas, 1935, parasite of Galea leucoblephara from Argentina, and G. kravetzi Sutton & Durette-Desset, 1995, parasite of Holochilus brasiliensis from Uruguay. It can be distinguished by shorter spicules, by the shape of the gubernaculum, by shorter uterine branches, and by a different number of ridges of the synlophe all along the body.     

Effects of Acute and Chronic Exposure to Predatory Cues on Spatial Learning Capabilities in the Subterranean Rodent Ctenomys talarum (Rodentia: Ctenomyidae)

Spatial learning, the cognitive ability that allows animals to efficiently locate food, partners or avoid predators, can be affected by various factors such as stress. Stressors represent a threat to the animal's homeostasis and trigger a set of physiological and behavioral changes known as stress response. The herbivorous rodent Ctenomys talarum (tuco‐tuco) inhabits underground complex gallery systems. Dispersal as well as food collection occurs on the surface, where they are exposed to terrestrial and aerial predators. We evaluated the effect of a natural stress factor, predation, on spatial learning of C. talarum. Additionally, we collected data on neutrophil/lymphocyte ratio, hematocrit, blood glucose, and plasma cortisol to assess physiological levels of stress. The acute exposure to direct cues indicating the presence of a predator (immobilization + cat urine) increased the time needed to reach the goal in a longitudinal labyrinth. The number of errors also increased albeit the difference was only marginally significant. The chronic exposure to predator cues (immobilization, cat urine, and cat fur) presented in an unpredictable order significantly increased both time and errors committed by tuco‐tucos during learning trials in the labyrinth. Results show the strong impact of predatory stress on the spatial abilities of C. talarum, a key cognitive process involved in most of their vital activities. They also highlight the importance of investigating wild species as regards the development of antipredatory defensive behaviors that contribute both to the avoidance of deleterious consequences of a direct attack and the influence on food search and mate localization performance.