Subterranean Rodent Research Articles

Field tests reveal acoustic variation of call types in a subterranean rodent, the Northern Mole Vole Ellobius talpinus

Abstract This study investigates acoustic variation of human-audible sonic (below 20 kHz) and human-inaudible ultrasonic (above 20 kHz) calls in a wild subterranean rodent, the Northern Mole Vole (Ellobius talpinus), under 3 call-eliciting tests conducted during captures for 1 day. The Contact-in-Tunnel Test modeled contacts of 2 individuals during digging earth in a burrow tunnel. The Restraint Test modeled restraint of an animal by a surrogate predator (human hand). The Release-to-Burrow Test modeled acoustic communication of many family members returned to their home burrow after their isolation for about 8 h, from morning to evening. We described 8 call types: 3 sonic, 3 ultrasonic, and 2 expanding from sonic to ultrasonic range of frequencies; 6 call types were described for the first time for this species. No relationship was found between acoustic parameters and proxies of body size (body mass and the width of 2 upper incisors). No sex differences were found in body size or the acoustic parameters. Different call types prevailed in different tests: wheeks and upsweeps were made during peaceful interactions; squeaks and squeals were related to animal discomfort during the Restraint Test; rasps were only made in Release-to-Burrow Tests when animals were plugging the burrow entrance; and variative calls did not show any relationship with type of test. Based on presence or absence of certain call types in the tests, we evaluate their potential communicative role in comparison with published data on vocal repertoires of other subterranean rodents.

Ultradian rhythms of activity in a wild subterranean rodent.

Many animals adapt their activity patterns to the best environmental conditions using daily rhythms. African mole-rats are among the mammals that have become models for studying how these rhythms can be entrained by light or temperature in experimental laboratory studies. However, it is unclear whether they exhibit similar circadian rhythms in their natural lightless, subterranean environment. In this study, we used biologging to investigate the activity rhythms of wild, highveld mole-rats. We show that their activity cycle exhibited an ultradian rhythm with a length between 4 and 8 h. On an individual level, mole-rats displayed about five activity bouts per day, occurring at various times during the day and night. On a population level, activity peaked in the afternoon, coinciding with the peak in ambient temperature. Our research suggests that wild subterranean mammals, which experience reduced environmental variation, are unlikely to show clear circadian rhythmicity in activity patterns. Instead, activity periods are distributed over several bouts throughout the day and night, and activity coincides with the peak in daily temperature. We propose that ultradian rhythms in activity may be more common than previously thought and discuss how physiological processes may generate differences in periodicity between laboratory and wild populations.

Introgression drives adaptation to the plateau environment in a subterranean rodent

BackgroundIntrogression has repeatedly been shown to play an important role in the adaptation of species to extreme environments, yet how introgression enables rodents with specialized subterranean lifestyle to acclimatize to high altitudes is still unclear. Myospalacinae is a group of subterranean rodents, among which the high-altitude plateau zokors (Eospalax baileyi) and the low-altitude Gansu zokors (E. cansus) are sympatrically distributed in the grassland ecosystems of the Qinghai-Tibet Plateau (QTP). Together, they provide a model for the study of the role of introgression in the adaptation of low-altitude subterranean rodents to high altitudes.ResultsApplying low-coverage whole-genome resequencing and population genetics analyses, we identified evidence of adaptive introgression from plateau zokors into Gansu zokors, which likely facilitated the adaptation of the latter to the high-altitude environment of the QTP. We identified positively selected genes with functions related to energy metabolism, cardiovascular system development, calcium ion transport, and response to hypoxia which likely made critical contributions to adaptation to the plateau environment in both plateau zokors and high-altitude populations of Gansu zokors.ConclusionsIntrogression of genes associated with hypoxia adaptation from plateau zokors may have played a role in the adaptation of Gansu zokors to the plateau environment. Our study provides new insights into the understanding of adaptive evolution of species on the QTP and the importance of introgression in the adaptation of species to high-altitude environments.

Natural Foraging Selection and Gut Microecology of Two Subterranean Rodents from the Eurasian Steppe in China.

As the most abundant group of mammals, rodents possess a very rich ecotype, which makes them ideal for studying the relationship between diet and host gut microecology. Zokors are specialized herbivorous rodents adapted to living underground. Unlike more generalized herbivorous rodents, they feed on the underground parts of grassland plants. There are two species of the genus Myospalax in the Eurasian steppes in China: one is Myospalax psilurus, which inhabits meadow grasslands and forest edge areas, and the other is M. aspalax, which inhabits typical grassland areas. How are the dietary choices of the two species adapted to long-term subterranean life, and what is the relationship of this diet with gut microbes? Are there unique indicator genera for their gut microbial communities? Relevant factors, such as the ability of both species to degrade cellulose, are not yet clear. In this study, we analyzed the gut bacterial communities and diet compositions of two species of zokors using 16S amplicon technology combined with macro-barcoding technology. We found that the diversity of gut microbial bacterial communities in M. psilurus was significantly higher than that in M. aspalax, and that the two species of zokors possessed different gut bacterial indicator genera. Differences in the feeding habits of the two species of zokors stem from food composition rather than diversity. Based on the results of Mantel analyses, the gut bacterial community of M. aspalax showed a significant positive correlation with the creeping-rooted type food, and there was a complementary relationship between the axis root-type-food- and the rhizome-type-food-dominated (containing bulb types and tuberous root types) food groups. Functional prediction based on KEGG found that M. psilurus possessed a stronger degradation ability in the same cellulose degradation pathway. Neutral modeling results show that the gut flora of the M. psilurus has a wider ecological niche compared to that of the M. aspalax. This provides a new perspective for understanding how rodents living underground in grassland areas respond to changes in food conditions.

Underground speciation: Unraveling the systematics and evolution of the highly diverse tuco-tucos (genus Ctenomys) with genomic data

Subterranean rodents of the genus Ctenomys (tuco-tucos) are endemic to South America and have experienced relatively recent radiation. There are about 67 recognized species that originated in approximately 1–2 MY. They stand out for their species richness, extraordinary chromosomal diversity, and wide range of habitat they occupy in the continent. Phylogenetic relationships among species of tuco-tucos have been challenging to resolve. Groups of closely-related species have been suggested, but their relationships must be resolved. This study estimates the phylogeny of the genus using massive sequencing, generating thousands of independent molecular markers obtained by RADseq, with a taxonomic sampling that includes 66% of the recognized species. The sequences obtained were mapped against the C. sociabilis genome, recovering up to 1,215 widely shared RAD loci with more than 19,000 polymorphic sites. Our new phylogenetic hypothesis corroborated the species groups previously proposed with cytochrome b gene sequences and provided a much greater resolution of the relationships among species groups. The frater group is sister to all other tuco-tucos, whereas some of the earlierliest proposals placed the sociabilis group as sister to all other tuco-tucos. Ctenomys leucodon, previously proposed as an independent lineage, is associated with the frater group with moderate statistical support. The magellanicus and mendocinus are sister groups in a major clade formed by the boliviensis, talarum, tucumanus, torquatus, and opimus groups. Ctenomys viperinus, included in the phylogeny for the first time, belongs to the tucumanus group. This multi-locus phylogenetic hypothesis provides insights into the historical biogeography of understanding this highly diverse genus.

Phylogenetic assessment within a species complex of a subterranean rodent (Geomys bursarius) with conservation implications for isolated subspecies.

Range contraction and expansion from glaciation have led to genetic divergence that may be particularly pronounced in fossorial species with low dispersal. The plains pocket gopher (Geomys bursarius) is a fossorial species that ranges widely across North America but has a poorly understood phylogeny. We used mitogenomes (14,996 base pairs) from 56 individuals across seven subspecies, plus two outgroup species, to assess genetic divergence from minimum spanning trees, measure genetic distances, and infer phylogenetic trees using BEAST. We found G. b. wisconsinensis was monophyletic with recent divergence. Further assessment is needed for G. b. major because it was paraphyletic and exhibited inconsistent groupings with other clades. Importantly, we identified G. b. illinoensis as being genetically distinct and monophyletic likely due to a unique colonization event eastward across the Mississippi River. Because G. b. illinoensis faces continued pressures from niche reduction and habitat loss, we recommend that G. b. illinoensis be considered an evolutionary significant unit warranting conservation actions to promote connectivity and restore suitable habitat. Such conservation efforts should benefit other grassland species including those originating from clades west of the Mississippi River that may also be evolutionary significant units.

Patterns of Genetic Diversity and Gene Flow Associated With an Aridity Gradient in Populations of Common Mole-rats, Cryptomys hottentotus hottentotus.

Genetic adaptation is the change of a population toward a phenotype that best fits the present ecological conditions of the environment it inhabits. As environmental conditions change, allele frequencies shift, resulting in different populations of the same species possessing genetic variation and divergent phenotypes. Cooperatively breeding common mole-rats (Cryptomys hottentotus hottentotus) inhabit environments along an aridity gradient in South Africa, which provides an opportunity for local genetic adaptations to occur. Using one mitochondrial gene (cytochrome b) and 3,540 SNP loci across the whole genome, we determined the phylogenetic relationship, population structure and genetic diversity of five populations of C. h. hottentotus located along an aridity gradient. Mitochondrial data identified population-specific clades that were less distinct in the two mesic populations, potentially indicating historical or recent gene flow, or the retention of ancestral haplotypes. Arid and semi-arid populations formed a distinct cluster from the non-arid populations. Genetic diversity and gene flow were higher in arid-dwelling individuals, suggesting greater connectivity and interactions between colonies in arid regions in comparison to mesic ones. Using an Aridity Index, we determined that isolation by environment, rather than isolation by geographical distance, best explains the genetic distance between the populations. Further analyses using target loci may determine if there are differing underlying genetic adaptations among populations of C. h. hottentotus. These analyses could help unravel population differences in response to environmental factors within a subspecies of bathyergid mole-rat and determine the adaptive capacity of this small nonmigratory subterranean rodent species in response to aridification in the face of climate change.

Pleistocene and modern distribution of the subterranean rodent Myospalax myospalax (Rodentia, Myospalacidae) in response to environmental factors

The question of the modern and past distribution of Siberian zokor Myospalax myospalax (Laxmann, 1773) continues to be an unresolved puzzle. This Western Siberian endemic species belongs to the family Myospalacidae, a group of subterranean rodents. The distribution of M. myospalax went through dramatic changes due to mass hunting in the first half of the 20th century and later development of agriculture. Because of this, data from various studies executed in different years do not always match, making it difficult to determine the natural limiting factors in the distribution of Siberian zokors. In turn, paleontological data from different regions are fragmentary and have not been summarized in a single study. We aimed to review the past and modern distribution of M. myospalax and examine its relationship with environmental factors such as climate and soils distribution. We hypothesized that this species may be a good indicator of past environmental conditions because of its special habitat characteristics. We gathered and revised published data to reconstruct the distribution before the anthropogenic influence of the 20th century and during the Pleistocene and Holocene epochs. The modern preanthropogenic range was compared with the distribution of soil complexes and provinces. We also examined M. myospalax molars from Late Pleistocene – Holocene localities and compared them with the modern population. The Siberian zokor distribution data provided herein will be useful for researchers from other regions who use fragmentary or doubtful data on the topic. We also identified climatic and soil parameters of M. myospalax habitat. These parameters can be used to reconstruct past environmental conditions from paleontological findings of the Siberian zokor.

Giant root-rat engineering and livestock grazing activities regulate plant functional trait diversity of an Afroalpine vegetation community in the Bale Mountains, Ethiopia

Disturbances from rodent engineering and human activities profoundly impact ecosystem structure and functioning. Whilst we know that disturbances modulate plant communities, comprehending the mechanisms through which rodent and human disturbances influence the functional trait diversity and trait composition of plant communities is important to allow projecting future changes and to enable informed decisions in response to changing intensity of the disturbances. Here, we evaluated the changes in functional trait diversity and composition of Afroalpine plant communities in the Bale Mountains of Ethiopia along gradients of engineering disturbances of a subterranean endemic rodent, the giant root-rat (Tachyoryctes macrocephalus Rüppell 1842) and human activities (settlement establishment and livestock grazing). We conducted RLQ (co-inertia analysis) and fourth-corner analyses to test for trait-disturbance (rodent engineering/human activities) covariation. Overall, our results show an increase in plant functional trait diversity with increasing root-rat engineering and increasing human activities. We found disturbance specific association with traits. Specifically, we found strong positive association of larger seed mass with increasing root-rat fresh burrow density, rhizomatous vegetative propagation negatively associated with increasing root-rat old burrow, and stolonifereous vegetative propagation positively associated with presence of root-rat mima mound. Moreover, both leaf size and leaf nitrogen content were positively associated with livestock dung abundance but negatively with distance from settlement. Overall, our results suggest that disturbances by rodents filter plant traits related to survival and reproduction strategies, whereas human activities such as livestock grazing act as filters for traits related to leaf economics spectrum along acquisitive resource-use strategy.

Spermatocytes are the terminals of germ cell differentiation in plateau zokor (Eospalax baileyi) during the non-breeding season.

Plateau zokor (Eospalax baileyi) is a subterranean rodent and seasonal breeder. During the non-breeding season, the testicles regress, leading to the arrest of spermatogenesis and loss of fertility. The identification of the specific germ cell type at which spermatogenesis is arrested, as well as potential regulatory factors during the non-breeding season, is important for understanding seasonal spermatogenesis in subterranean species. This study analyzed genes in spermatocytes of plateau zokor by referring to single-cell RNA results in mice. We discovered that spermatogenesis is arrested at the spermatocyte during the non-breeding season, which was corroborated via immunofluorescence staining results. The analysis of gene expression during different stages of meiotic prophase I has revealed that germ cell development may be arrested, starting from zygonema, during the non-breeding season. Meanwhile, we discovered that the apoptosis genes were up-regulated, leading to apoptosis in spermatocytes. To confirm that the germ cell differentiation was blocked during the non-breeding season due to a decrease in the androgen level, we used androgen receptor antagonist (flutamide) to intervene in the breeding season and found that the inner diameter of the seminiferous tubules was significantly reduced, spermatogenesis was arrested, and spermatocytes underwent apoptosis. This study revealed that spermatocytes are the terminal of germ cell differentiation in plateau zokor during the non-breeding season and that the arrest of differentiation is attributed to a decline in androgen levels. Our results complement the theoretical basis of seasonal reproduction in plateau zokor.

Five new unexpected populations of endangered tuco-tuco Ctenomys rionegrensis (Rodentia, Ctenomyidae) help understanding its distribution and historical biogeography

In this study, we conducted a survey of newly discovered populations of tuco-tuco (subterranean rodents of the genus Ctenomys) in the Entre Ríos province, in an area characterized by its unexplored nature and its climatic and biogeographic complexity within Argentina, which includes two National Parks. We characterize the nucleotide sequences of the cytochrome-b gene, revealing the presence of seven novel haplotypes within Ctenomys rionegrensis, a species known to inhabit both sides of the Uruguay River. Through Bayesian analyses, we estimated the divergence times of the oldest lineages of C. rionegrensis, as well as those of the haplotypes located east of the Uruguay River, dating back approximately 630,000 years before present (ybp) and 526,000 ybp, respectively. These estimates correspond with significant paleogeographic events in the region. Our findings may raise questions regarding the taxonomic classification of the species and suggest potential modifications to its current endangered status as designated by the International Union for Conservation of Nature (IUCN). Consequently, this research provides valuable insights that may inform future revisions of the species' conservation status and guide the development of informed management strategies/policies.

Effect of an herbivorous subterranean rodent on vegetation in relation to primary productivity

AbstractSubterranean rodents modify the surrounding environment being classified, in some cases, as keystone species and/or ecosystem engineers. This role could be context‐dependent if the changes produced shift throughout the species distribution range and are stronger under certain environmental conditions. Our objective was to analyse whether the effect of Ctenomys mendocinus on vegetation cover is context‐dependent. Given that primary productivity may increase plants' ability to tolerate or compensate following herbivory, we hypothesize that the effect of C. mendocinus on vegetation cover will be context‐dependent along a primary productivity gradient, with smaller effects in highly productive environments and larger effects in less productive ones. We compared the effect of C. mendocinus on plant cover among four contrasting environments and found that it depended on primary productivity in a predictable manner. In low productivity environments, the rodent significantly reduces vegetation cover, while it has no discernible effect in highly productive ones. These findings suggest that the effect of C. mendocinus on plant cover depends on primary productivity level and highlights the importance of accounting for the underlying environmental factors that influence the intensity of C. mendocinus–plant interaction.

Partitioning genetic structure of a subterranean rodent at multiple spatial scales: accounting for isolation by barriers, distance, and environment

ContextUnderstanding genetic structure at multiple spatial scales and identifying drivers of genetic isolation are important for developing comprehensive conservation plans including for grassland conservation efforts. However, few studies account for multiple genetic isolation processes nor partition genetic variance among these processes.ObjectivesWe assess key processes that can create spatial genetic patterns including isolation by barrier (IBB), isolation by distance (IBD), and isolation by environment (IBE) for a widespread pocket gopher species (Geomys bursarius) and a spatially restricted subspecies (Geomys bursarius illinoensis). We further partition genetic variation to each isolating effect and identify genetic variation that was shared between processes.MethodsWe used seven microsatellites to determine spatial genetic clustering and identify environmental factors impacting genetic similarities. Then, we used redundancy analysis to partition variance explained by IBB, IBD, and IBE.ResultsMajor rivers including the Mississippi River acted as barriers and explained the most genetic variation across the species. In contrast, IBD explained the most genetic variation for G. b. illinoensis. Gophers had genetic associations to soil sand percent and soil color, but IBE uniquely explained a small amount of genetic structure for G. bursarius, with additional variation shared with other isolating processes.ConclusionsGopher genetic structure resulted from barriers, distance, and environmental factors at the species range as well as for a subspecies’ region, but the relative amount of genetic variance assigned to unique isolating processes differed between scales. Delineation of conservation units should consider major rivers as natural boundaries, and finer-scale management should identify and protect areas close to source populations with similar soil friability. Our study exemplifies how analyzing gene flow at rangewide and regional scales can aid managers in developing localized strategies that fit within broader conservation units.

Body temperature and locomotor activity of social subterranean mole voles (Ellobius talpinus) in winter

To find out whether a social subterranean rodent—the northern mole vole (Ellobius talpinus)—hibernates in winter, nine individuals from Southern Siberia were captured in late autumn and implanted with loggers [that constantly recorded body temperature (Tb) and locomotor activity] and then released. Eight of them were recaptured the following spring. From October to April, the animals’ Tb never dropped below 33 °C, although cosinor analysis revealed a decrease in mesor values and in the amplitude of daily fluctuations of Tb and activity in winter months. Spectral density of circadian rhythms of both indexes also diminished in winter. The magnitude of Tb and fluctuations of activity differed between the two studied familial groups, probably due to their unequal numbers of individuals, which could affect the total heat production. The levels and patterns of temperature and activity fluctuations observed in winter rule out the possibility of hibernation in this species.

Same scenario, different scripts: Landscape genetics in two codistributed subterranean rodents of the genus Ctenomys

AbstractSubterranean rodents of the genus Ctenomys typically occupy fragmented habitats, many currently altered by anthropogenic development. These changes affect functional connectivity among individuals, reducing gene flow levels. This study assessed the functional connectivity of two sympatric species of subterranean rodents, Ctenomys australis and Ctenomys talarum, examining the impact of landscape changes on their population genetic structure at a fine spatial scale. We conducted a spatially continuous sampling over 12 km of coastline in Southeastern Buenos Aires Province, Argentina, genotyping 91 and 106 individuals of C. australis and C. talarum, respectively, using 10–12 microsatellite loci. We applied various spatial layers characterizing both species' habitats to evaluate the landscape configuration's effect on individual gene flow. We employed Bayesian genetic clustering methods to infer population structure levels. Ctenomys talarum showed greater structure than C. australis. NDVI temporal variation was the main factor influencing C. australis' genetic structure, whereas suitable habitat, linked to the current landscape configuration, was the most significant factor in shaping C. talarum's genetic structure. Differences in dispersal capacity and habitat specificity appear to have influenced the population genetic structures of these species. The results indicated varying sensitivities to landscape changes; temporal landscape variations primarily impacted C. australis' genetic connectivity, whereas for C. talarum, the current landscape configuration was more influential.

A new camera-trapping device, the Campascope, to study feeding behaviour of subterranean rodents

A new camera-trapping device, the Campascope, to study feeding behaviour of subterranean rodents

Genomic structural variation is associated with hypoxia adaptation in high-altitude zokors.

Zokors, an Asiatic group of subterranean rodents, originated in lowlands and colonized high-elevational zones following the uplift of the Qinghai-Tibet plateau about 3.6 million years ago. Zokors live at high elevation in subterranean burrows and experience hypobaric hypoxia, including both hypoxia (low oxygen concentration) and hypercapnia (elevated partial pressure of CO2). Here we report a genomic analysis of six zokor species (genus Eospalax) with different elevational ranges to identify structural variants (deletions and inversions) that may have contributed to high-elevation adaptation. Based on an assembly of a chromosome-level genome of the high-elevation species, Eospalax baileyi, we identified 18 large inversions that distinguished this species from congeners native to lower elevations. Small-scale structural variants in the introns of EGLN1, HIF1A, HSF1 and SFTPD of E. baileyi were associated with the upregulated expression of those genes. A rearrangement on chromosome 1 was associated with altered chromatin accessibility, leading to modified gene expression profiles of key genes involved in the physiological response to hypoxia. Multigene families that underwent copy-number expansions in E. baileyi were enriched for autophagy, HIF1 signalling and immune response. E. baileyi show a significantly larger lung mass than those of other Eospalax species. These findings highlight the key role of structural variants underlying hypoxia adaptation of high-elevation species in Eospalax.

Numerous insertions of mitochondrial DNA in the genome of the northern mole vole, Ellobius talpinus

BackgroundEllobius talpinus is a subterranean rodent representing an attractive model in population ecology studies due to its highly special lifestyle and sociality. In such studies, mitochondrial DNA (mtDNA) is widely used. However, if nuclear copies of mtDNA, aka NUMTs, are present, they may co-amplify with the target mtDNA fragment, generating misleading results. The aim of this study was to determine whether NUMTs are present in E. talpinus.Methods and resultsPCR amplification of the putative mtDNA CytB-D-loop fragment using ‘universal’ primers from 56 E. talpinus samples produced multiple double peaks in 90% of the sequencing chromatograms. To reveal NUMTs, molecular cloning and sequencing of PCR products of three specimens was conducted, followed by phylogenetic analysis. The pseudogene nature of three out of the seven detected haplotypes was confirmed by their basal positions in relation to other Ellobius haplotypes in the phylogenetic tree. Additionally, ‘haplotype B’ was basal in relation to other E. talpinus haplotypes and found present in very distant sampling sites. BLASTN search revealed 195 NUMTs in the E. talpinus nuclear genome, including fragments of all four PCR amplified pseudogenes. Although the majority of the NUMTs studied were short, the entire mtDNA had copies in the nuclear genome. The most numerous NUMTs were found for rrnL, COXI, and D-loop.ConclusionsNumerous NUMTs are present in E. talpinus and can be difficult to discriminate against mtDNA sequences. Thus, in future population or phylogenetic studies in E. talpinus, the possibility of cryptic NUMTs amplification should always be taken into account.

Genetic footprints of Quaternary climatic fluctuations on the endangered Tuco-tuco-das-dunas (Ctenomys flamarioni)

Abstract The biogeographic history of a species results from responses to past and current processes, and understanding those responses at both temporal scales is essential. We explored phylogeographic and current genetic variation structure in Ctenomys flamarioni—a subterranean rodent that inhabits a small region of the coastal plain of Brazil—and contrasted the roles of “present-day niche suitability” versus “historical climate stability” to understand current and past intraspecific genetic diversity. We used both mitochondrial DNA sequences (concatenated Cytb and D-loop, n = 78) and nuclear DNA (9 microsatellites loci, n = 154) molecular markers for individuals across the entire distribution of the species. We used phylogeographic trees, Bayesian clustering, and haplotype networks to explore genetic variation and diversity. We correlated genetic diversity with measures of current niche suitability and potential areas of Late Quaternary paleostability. Phylogeographic patterns confirmed low levels of genetic diversity structured at different hierarchical levels. We also found a weak but significant pattern of isolation by distance, indicating that geographical distance partially modulates genetic differences among populations. We also observed a positive correlation between genetic diversity and climate paleostability for microsatellites at local and regional scales. However, we found no significant association between genetic diversity and niche suitability for microsatellites at local or regional scales. We observed several signatures of bottleneck and population expansion at different geographic scales. Our results suggest that Quaternary climatic fluctuations—acting together with habitat suitability and other contemporary factors—played a fundamental role in elucidating the evolutionary history of the species—including patterns of historical dispersal, and current patterns of habitat occupation and genetic structure. In addition, based on our molecular and environmental data sets from the across the range of the species and considering the restricted endemism of C. flamarioni, we emphasize the urgency of conservation actions to protect this endangered species.

A clock for all seasons in the subterranean.

In 1976, Pittendrigh and Daan established a theoretical framework which has coordinated research on circadian clock entrainment and photoperiodism until today. The "wild clocks" approach, which concerns studying wild species in their natural habitats, has served to test their models, add new insights, and open new directions of research. Here, we review an integrated laboratory, field and modeling work conducted with subterranean rodents (Ctenomys sp.) living under an extreme pattern of natural daily light exposure. Tracking animal movement and light exposure with biologgers across seasons and performing laboratory experiments on running-wheel cages, we uncovered the mechanisms of day/night entrainment of the clock and of photoperiodic time measurement in this subterranean organism. We confirmed most of the features of Pittendrigh and Daan's models but highlighted the importance of integrating them with ecophysiological techniques, methodologies, and theories to get a full picture of the clock in the wild. This integration is essential to fully establish the importance of the temporal dimension in ecological studies and tackling relevant questions such as the role of the clock for all seasons in a changing planet.