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.     

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.     

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.     

Historical demography and spatial genetic structure of the subterranean rodent Ctenomys magellanicus in Tierra del Fuego (Argentina)

Ctenomys (tuco‐tuco) is the most numerous genus of South American subterranean rodents and one of the most genetically diverse clades of mammals known. In particular, the genus constitutes a very interesting model for evolutionary studies of genetic divergence and conservation. Ctenomys magellanicus is the southernmost species of the group and the only one living in Isla Grande de Tierra del Fuego (Argentina). This species presents two chromosomal forms (Cm34 and Cm36) fragmented into demes distributed from the north region (steppe) to the south region (ecotone) of the island, respectively; no hybrids or overlapping areas were detected. To study the historical demography and the spatial genetic structure of the C. magellanicus population we used mitochondrial DNA (mtDNA) (D‐loop and cytochrome b) and microsatellite loci. Nine mtDNA haplotypes were identified, three of them belonging to the north and the other six to the south. Shared haplotypes between regions were not detected. mtDNA and microsatellite genotypes showed a marked pattern of population structure with low values of genetic flow between regions. The south is made up of small populations or isolated demes making up an endogamic metapopulation with unique alleles and haplotypes. Also, the results suggest a northward expansion process starting from an ancestral haplotype from the south. That population might have lived at a refuge through the adverse Pleistocene environmental conditions that took place at Tierra del Fuego. Results of this study are relevant to the conservation of C. magellanicus, suggesting that each region (north and south) might be considered as an Evolutionarily Significant Unit. © 2013 The Linnean Society of London     

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.     

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.     

Population structure and landscape genetics of two endangered frog species of genus Odorrana: different scenarios on two islands

Isolation by distance and landscape connectivity are fundamental factors underlying speciation and evolution. To understand how landscapes affect gene flow and shape population structures, island species provide intrinsic study objects. We investigated the effects of landscapes on the population structure of the endangered frog species, Odorrana ishikawae and O. splendida, which each inhabit an island in southwest Japan. This was done by examining population structure, gene flow and demographic history of each species by analyzing 12 microsatellite loci and exploring causal environmental factors through ecological niche modeling (ENM) and the cost-distance approach. Our results revealed that the limited gene flow and multiple-population structure in O. splendida and the single-population structure in O. ishikawae were maintained after divergence of the species through ancient vicariance between islands. We found that genetic distance correlated with geographic distance between populations of both species. Our landscape genetic analysis revealed that the connectivity of suitable habitats influences gene flow and leads to the formation of specific population structures. In particular, different degrees of topographical complexity between islands are the major determining factor for shaping contrasting population structures of two species. In conclusion, our results illustrate the diversification mechanism of organisms through the interaction with space and environment. Our results also present an ENM approach for identifying the key factors affecting demographic history and population structures of target species, especially endangered species.     

Craniodental and forelimb specializations for digging in the South American subterranean rodent Ctenomys (Hystricomorpha,Ctenomyidae)

We explored the distribution of tooth- and scratch-digging specializations in species of the subterranean rodent Ctenomys (tuco-tucos) from diverse environments and representing different clades. Principal component analysis of craniodental and postcranial indexes with functional relevance showed that specializations for tooth-digging on one hand, and scratch- digging on the other, formed two uncorrelated groups of variables; functionally significant enamel traits varied concurrently with the tooth-digging specialization axis. Species occupied all sectors of the morphospace showing that craniodental and forelimb specializations have not been mutually exclusive in the evolution of the genus.     

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.     

Role of maternal odors on foraging behavior during postnatal development in a solitary subterranean rodent Ctenomys talarum

We investigated the role of maternal odors emanating from excretory deposits and/or glandular secretions during the postnatal development of foraging and related behaviors in young Los Talas’ tuco-tucos (Ctenomys talarum), a solitary rodent, under seminatural conditions. During cafeteria tests, we offered them two of the grasses most preferred by adults of this species (bromegrass, Bromus unioloides and panicgrass, Panicum racemosum). We scent marked one dietary option in a treatment group, and the other option in a second treatment group, keeping a third group with no odors as control. Pups did not show to prefer a special grass in particular, and maternal odors showed no effect on the behavioral variables evaluated in this study. When they reached their weaning age, they showed an ontogenetic change in food preferences, where they preferred bromegrass, and maternal odors influenced negatively on the consumption of panicgrass. During dispersal, preference for bromegrass was expressed independently of the presence of maternal odors. Overall, their effect was less pronounced than age’s effect, and it was evident in only a subset of the conducted experiments. This study shows that the influence of maternal odors is not essential for the establishment of feeding or site preferences in this species in seminatural conditions, contrarily to what was observed in other studies performed with social mammal species (i.e., rats and rabbits). It is suggested that other factors (e.g., individual learning) might influence the observed preferences.     

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.     

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.     

Population genetics of the endangered Knysna seahorse,Hippocampus capensis

The evolutionary history of the endangered Knysna seahorse, Hippocampus capensis, and the extent of gene flow among its three known populations, were investigated using 138 mitochondrial DNA control region sequences. Similarly high levels of genetic diversity were found in two of the populations (Knysna and Keurbooms Estuaries), whereas diversity in the third population (Swartvlei Estuary) was lower. Although most haplotypes are shared between at least two populations, based on the haplotype frequency distributions the three assemblages constitute distinct management units. The extant population structure of H. capensis suggests that the Knysna seahorse originated in the large Knysna Estuary. The presence of seahorses in the two smaller estuaries is either the result of a vicariance event at the beginning of the present interglacial period, colonization of the estuaries via the sea, or a combination of the two.     

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.     

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     

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.