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.     

The influence of foraging mode and arid adaptation on the basal metabolic rates of burrowing mammals

Two competing but nonexclusive hypotheses to explain the reduced basal metabolic rate (BMR) of mammals that live and forage underground (fossorial species) are examined by comparing this group with burrowing mammals that forage on the surface (semifossorial species). These hypotheses suggest that the low BMR of fossorial species either compensates for the enormous energetic demands of subterranean foraging (the cost-of-burrowing hypothesis) or prevents overheating in closed burrow systems (the thermal-stress hypothesis). Because phylogentically informed allometric analysis showed that arid burrowing mammals have a significantly lower BMR than mesic ones, fossorial and semifossorial species were compared within these groups. The BMRs of mesic fossorial and semifossorial mammals could not be reliably distinguished, nor could the BMRs of large (>77 g) arid fossorial and semifossorial mammals. This finding favours the thermal-stress hypothesis, because the groups appear to have similar BMRs despite differences in foraging costs. However, in support of the cost-of-burrowing hypothesis, small (<77 g) arid fossorial mammals were found to have a significantly lower BMR than semifossorial mammals of the similar size. Given the high mass-specific metabolic rates of small animals, they are expected to be under severe energy and water stress in arid environments. Under such conditions, the greatly reduced BMR of small fossorial species may compensate for the enormous energetic demands of subterranean foraging.     

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 VO2 during digging and resting at ambient temperature (Ta) below, within, and above thermoneutrality. Digging metabolic rate was lowest at Ta within the thermoneutral zone and increased at both lower and higher temperatures, but body temperature (Tb) remained constant at all Tas. 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 Tb during digging.     

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.     

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.     

Metabolic rate and thermoregulation in two species of tuco-tuco, Ctenomys talarum and Ctenomys australis (Caviomorpha, Octodontidae)

1. Resting metabolic rate and body temperature in function of ambient temperature were determined for two species of Ctenomys. 2. Oxygen consumption was lowest between 25 and 30 degrees C and was 0.946 +/- 0.030 and 0.968 +/- 0.022 in Ctenomys talarum (from Mar de Cobo and Necochea, respectively). Resting metabolic rate was 0.343 +/- 0.053 at 30 C in C. australis. 3. Mean rectal temperature at thermoneutrality was 36.1 +/- 0.13 and 37.3 +/- 0.17 in C. talarum and C. australis, respectively. 4. Limited thermoregulation occurred in C. talarum down to 20 degrees C but C. australis maintained body temperature down to 10 degrees C. 5. Both species of tuco-tucos became hyperthermic at ambient temperatures above thermoneutrality.     

Seasonal changes in body composition of Ctenomys talarum (Rodentia: Octodontidae): an herbivore subterranean rodent

Ctenomys talarum is a subterranean herbivorous rodent whose burrow systems exhibit particular characteristics, distinct from other subterranean environments. We studied seasonal variation in body composition of C. talarum in relation to energetic requirements. Body lipid content seasonally changed in C. talarum, related to reproductive cycle and thermorregulatory mechanisms. A decrease in protein body content was found only in spring. Ash content of females was lowest when most of them are in post partum estro. Observed variations in water body content could be associated with plant water content and/or metabolic regulation. Our results show the occurrence of seasonal variations in body composition in C. talarum, which could be related to the high cost of reproduction and the subterranean life style of this species.     

Functional morphology and paleobiology of the pliocene rodent Actenomys (Caviomorpha: Octodontidae): the evolution to a subterranean mode of life

The Pliocene caviomorph rodent Actenomys has long been recognized as an early fossorial representative of the subfamily Ctenomyinae (Octodontidae), which includes one living genus, Ctenomys (tuco-tucos), and several species widely distributed in South America. To assess the de gree of specialization for digging in Actenomys , we performed morphological comparisons with other octodontid genera (Octodon, Spalacopus , and Ctenomys) of known mode of life and behaviour. As a whole, our results indicate that, in terms of morphological specializations for digging, Actenomys occupies an intermediate position between Octodon , a generalized semi-fossorial rodent which forages above ground, and Ctenomys-Spalacopus , two highly specialized subterranean forms. The position of the deltoid process (humerus) and the length of the olecranon process (ulna)–two traits which affect the out-forces exerted by several forelimb muscles–were in Actenomys intermediate between non-subterranean and subterranean taxa. The skull, particularly the rostrum, appears to be strong, and sagittal and nuchal crests are well marked. The zygomatic arches arc as flared as those of the generalized Octodon. Notably, the upper and lower incisors of Actenomys were extremely procumbent, as in many highly-specialized chisel-tooth digging species. Based upon the stratigraphic and sedimentological analysis of the palaeosoils containing its fossil remains, we suggest that Actenomys lived in an environment of moderate to hig primary productivity. The texture of the palaeosoils indicate that theywere hard and highly cohesive. This situation, which contrasts with that observed in living Ctenomyinae, has relevant implications for burrowing cost. The integration of morphological and palaeoenvironmental data allowed testing of hypotheses about the palaeobiological attributes of this ancestral ctenomyine.     

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.     

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.     

Phenotypic flexibility in basal metabolic rate and the changing view of avian physiological diversity: a review

Comparative analyses of avian energetics often involve the implicit assumption that basal metabolic rate (BMR) is a fixed, taxon-specific trait. However, in most species that have been investigated, BMR exhibits phenotypic flexibility and can be reversibly adjusted over short time scales. Many non-migrants adjust BMR seasonally, with the winter BMR usually higher than the summer BMR. The data that are currently available do not, however, support the idea that the magnitude and direction of these adjustments varies consistently with body mass. Long-distance migrants often exhibit large intra-annual changes in BMR, reflecting the physiological adjustments associated with different stages of their migratory cycles. Phenotypic flexibility in BMR also represents an important component of short-term thermal acclimation under laboratory conditions, with captive birds increasing BMR when acclimated to low air temperatures and vice versa. The emerging view of avian BMR is of a highly flexible physiological trait that is continually adjusted in response to environmental factors such as temperature. The within-individual variation observed in avian BMR demands a critical re-examination of approaches used for comparisons across taxa. Several key questions concerning the shapes and other properties of avian BMR reaction norms urgently need to be addressed, and hypotheses concerning metabolic adaptation should explicitly account for phenotypic flexibility.     

Basal metabolism is correlated with habitat productivity among populations of degus (Octodon degus)

Several competing hypotheses attempt to explain how environmental conditions affect mass-independent basal metabolic rate (BMR) in mammals. One of the most inclusive is the hypothesis that associates BMR with food habits, including habitat productivity. The effects of food habits have been widely investigated at the interspecific level, and variation between individuals and populations has been largely ignored. Intraspecific analysis of physiological traits has the potential to compensate for many pitfalls associated with interspecific analyses and serve as a useful approach for evaluating hypotheses regarding metabolic adaptation. Here we tested the effects of climatic variables (mean annual rainfall = PP, mean annual temperature = T_A), net primary productivity (NPP) and the de Martonne index (DMi) of aridity on mass-independent BMR among four populations of the caviomorph rodent Octodon degus along a geographic gradient in Chile. BMR was measured on animals maintained in a common garden acclimation set-up, thus kept under the same environment and diet quality for at least 6 months. Mass-independent BMR was significantly different among degu populations showing a large intraspecific spread in metabolic rates. A very large fraction of interpopulational variability in mass-independent BMR was explained by NPP, PP and DMi. Our results were conclusive about the effects of habitat productivity on setting the level of mass-independent BMR at the intraspecific–interpopulational level.     

Relationship between helminth parasites and demographic attributes of a population of the subterranean rodent Ctenomys talarum (Rodentla: Octodontidae)

The helminth parasite fauna of a natural population of the octodontid, Ctenomys talarum, was studied. Parasites that were found included the nematodes Heligmostrongylus sp. and Trichuris sp. Total prevalence of parasitism was 92.3%, mean intensity of infection was 22.7 worms, and mean abundance was 21 worms. Prevalence and mean abundance of infection with Heligmostrongylus sp. were higher in C. talarum males relative to females. Ecological and physiological causes, as well as the mating system of the host species, influence the likelihood of sex differences in parasite infection. The low parasite burden and diversity of C. talarum are associated with restrictions imposed by the subterranean habitat and with life-history traits of these rodents. Whether these findings apply to other Ctenomys spp. is unknown.     

Automatic data recording of circadian rhythms

This paper illustrates a method for automatic data recording using the printer port of personal computer and software designed ad hoc. The system was tested by measuring circadian rhythms of activity in the subterranean rodent Ctenomys talarum. Data is recorded in a text-only comma-delimited file, and displayed on screen.     

Allometry and adaptation in the long bones of a digging group of rodents (Ctenomyinae)

Previous studies of rodent appendicular morphology suggest that digging activity induces changes in long bones, producing shorter and thicker structures. Subsequent hypotheses have been tested in Ctenomyinae, a group of octodontid rodents globally adapted to subterranean life. Slopes of the equations calculated for extant animals and their corresponding confidence intervals agree with expectations in almost all cases. Results on fossil taxa are less clear, but suggest a morphocline from a plesiomorphic condition of the appendicular skeleton, present in the fossil genera, departing little from that of the current epigeous rodents, to a more derived long bone design in the species of the living genus Ctenomys , in accordance with their digging activity.     

Decreased glucose tolerance but normal blood glucose levels in the field in the caviomorph rodent Ctenomys talarum: the role of stress and physical activity

Hystricomorph rodents have a divergent insulin molecule with only 1-10% of the biological activity in comparison to other mammalian species. In this study, we used the subterranean rodent Ctenomys talarum as a model and performed blood glucose tolerance tests (GTTs) with trained and untrained individuals to evaluate blood glucose regulation and the possible role of physical activity as a compensatory mechanism. Additionally, we evaluated the variations in blood glucose during acute and chronic stress and gathered data in the field to evaluate natural-occurring variations in blood glucose levels. The GTTs showed that C. talarum have a diminished capacity of regulating blood glucose levels in comparison to other mammals and suggest that unexplored differences in the compensatory mechanisms, insulin structure and/or glucose transporters exist within species of hystricomorph rodents. However, blood glucose levels in the field stayed within the normal mammalian range. Physical activity did not prove to be a compensatory mechanism for blood glucose regulation. The individuals did not display important increases in blood glucose after acute stressors and managed to adequately regulate blood glucose during chronic stress. We suggest that the species may not face a selective pressure favoring a more tightly, mammalian like, capacity of regulating blood glucose levels.     

Basal metabolic rate in carnivores is associated with diet after controlling for phylogeny

Studies of basal metabolic rate (BMR), the minimum metabolic rate of postabsorptive, inactive endotherms while in their rest phase and thermal neutral zone, have contributed significantly to our understanding of animal energetics. Besides body mass, the main determinant of BMR, researchers have invoked diet and phylogenetic history as important factors that influence BMR, although their relative importance has been controversial. For 58 species within the Carnivora, we tested the hypothesis that BMR is correlated with home range size, a proxy for level of activity, and diet, using conventional least squares regression (CLSR) and regression based on phylogenetic independent contrasts (PIC). Results showed that BMR of Carnivora was positively correlated with home range size after controlling for body mass, regardless of the statistical method employed. We also found that diet and mass-adjusted home range size were correlated. When we simultaneously tested the effect of diet and mass-adjusted home range on mass-adjusted BMR, home range size was insignificant because of its colinearity with diet. Then we eliminated home range size from our model, and diet proved to be significant with both CLSR and PIC. We concluded that species that eat meat have larger home ranges and higher BMR than species that eat vegetable matter. To advance our understanding of the potential mechanisms that might explain our results, we propose the "muscle performance hypothesis," which suggests that selection for different muscle fiber types can account for the differences in BMR observed between meat eaters and vegetarian species within the Carnivora.     

Bioenergetics of reproduction and pup development in a subterranean rodent (Ctenomys talarum)

The objective of this study was to evaluate the maternal costs of reproduction and pup development in the subterranean rodent Ctenomys talarum (Thomas 1898). Statistical differences were detected in whole-animal metabolic rates between nonreproductive and pregnant or lactating females. Whole-animal metabolic rates during pregnancy and lactation were 128% and 151% of the resting metabolic rate (RMR) observed in nonreproductive females. The total additional energy cost of reproduction (above the nonreproductive level) was similar for both the gestation and lactation periods. Mass-specific RMR revealed an upregulation of cell or tissue metabolism during lactation but not during gestation. The mass-specific metabolic rate of pups was 237% of the adults' metabolic rates. No differences were observed in body temperature among nonreproductive, pregnant, or lactating females. No differences were detected in body mass at birth among pups from litters with different numbers of nestlings. Pups increased their body temperature, reaching adult temperature at 30 d of age, when they were near weaning. Milk constituted the exclusive food for pups until they started eating solid food at 10 d old. Suckling time decreased with age of pups, and at the same time, mother chases directed toward their pups increased. These reproductive characteristics may contribute to successful existence in a subterranean habitat.     

Digestive flexibility in females of the subterranean rodent ctenomys talarum in their natural habitat

We studied the occurrence of digestive strategies at different levels in females of the subterranean herbivorous rodent Ctenomys 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(sucrase, maltase and N-aminopeptidase) in small intestine in females seasonally caught. Females of C. talarum did not show seasonal variations in the mass of the different parts of the gastrointestinal tract. In nonreproductive females large intestine was longer in autumn, whereas reproductive females did not show seasonal variations in the length of the different parts of the gut. Females of C. talarum exhibited a high sucrose, maltase and N-aminopeptidase activity in small intestine, although these activities were higher in small intestine of females caught in autumn (nonreproductive) than in females caught in winter (reproductive). The results show that C. talarum females exhibit characteristics in the gut at the morphological and biochemical level, which could represent digestive strategies to face the constraints imposed by their costly particular way of life.     

Intraspecific variability in the Basal metabolic rate: testing the food habits hypothesis

Several competing hypotheses attempt to explain how environmental conditions affect mass-independent basal metabolic rate (BMR) in mammals. One of the most inclusive and yet debatable hypotheses is the one that associates BMR with food habits, including habitat productivity. These effects have been widely investigated at the interspecific level under the assumption that for any given species all traits are fixed. Consequently, the variation among individuals is largely ignored. Intraspecific analysis of physiological traits has the potential to compensate for many of the pitfalls associated with interspecific analyses and, thus, to be a useful approach for evaluating hypotheses regarding metabolic adaptation. In this study, we investigated the effects of food quality, availability, and predictability on the BMR of the leaf-eared mouse Phyllotis darwini. BMR was measured on freshly caught animals from the field, since they experience natural seasonal variations in environmental factors (and, hence, variations in habitat productivity) and diet quality. BMR was significantly correlated with the proportion of dietary plants and seeds. In addition, BMR was significantly correlated with monthly habitat productivity. Path analysis indicated that, in our study, habitat productivity was responsible for the observed changes in BMR, while diet per se had no effect on this variable.