Energy allocation is revealed while behavioural performance persists after fire disturbance.

Metabolic physiology and animal behaviour are often considered to be linked, positively or negatively, according to either the performance or allocation models. Performance seems to predominate over allocation in natural systems, but the constraining environmental context may reveal allocation limitations to energetically expensive behaviours. Habitat disturbance, such as the large-scale fire that burnt wetlands of Biebrza National Park (NE Poland), degrades natural ecosystems. It arguably reduces food and shelter availability, modifies predator-prey interactions, and poses a direct threat for animal survival, such as that of the wetland specialist root vole Microtus oeconomus. We hypothesized that fire disturbance induces physiology-behaviour co-expression, as a consequence of changed environmental context. We repeatedly measured maintenance and exercise metabolism, and behavioural responses to the open field, in a root voles from post-fire and unburnt locations. Highly repeatable maintenance metabolism and distance moved during behavioural tests correlated positively, but relatively labile exercise metabolism did not covary with behaviour. At the same time, voles from a post-fire habitat had higher maintenance metabolism and moved shorter distances than voles from unburnt areas. We conclude there is a prevalence of the performance mechanism, but simultaneous manifestation of context-dependent allocation constraints of the physiology-behaviour covariation after disturbance. The last occurs at the within-individual level, indicating the significance of behavioural plasticity in the context of environmental disturbance.

Unraveling phylogenetic relationships and species boundaries in the arid adapted Gerbillus rodents (Muridae: Gerbillinae) by RAD-seq data.

Gerbillus is one of the most speciose genera among rodents, with ca. 51 recognized species. Previous attempts to reconstruct the evolutionary history of Gerbillus mainly relied on the mitochondrial cyt-b marker as a source of phylogenetic information. In this study, we utilize RAD-seq genomic data from 37 specimens representing 11 species to reconstruct the phylogenetic tree for Gerbillus, applying concatenation and coalescence methods. We identified four highly supported clades corresponding to the traditionally recognized subgenera: Dipodillus, Gerbillus, Hendecapleura and Monodia. Only two uncertain branches were detected in the resulting trees, with one leading to diversification of the main lineages in the genus, recognized by quartet sampling analysis as uncertain due to possible introgression. We also examined species boundaries for four pairs of sister taxa, including potentially new species from Morocco, using SNAPP. The results strongly supported a speciation model in which all taxa are treated as separate species. The dating analyses confirmed the Plio-Pleistocene diversification of the genus, with the uncertain branch coinciding with the beginning of aridification of the Sahara at the the Plio-Pleistocene boundary. This study aligns well with the earlier analyses based on the cyt-b marker, reaffirming its suitability as an adequate marker for estimating genetic diversity in Gerbillus.

Diversity of Rickettsia spp. in ticks from wild mammals of Morocco and Mauritania.

Ticks are known as vectors and reservoirs of rickettsiae and, wildlife vertebrate hosts as suitable dispersers of ticks contributing to the life cycle of rickettsial agents in nature. In the herein study, the presence of rickettsiae was investigated in ticks from wild mammals (Gerbillus and Jaculus, Vulpes rueppellii, Canis anthus, Felis lybica and Felis margarita) in Mauritania and Morocco. Morphological and molecular analysis of ticks allowed their identification as Rhipicephalus sanguineus sensu lato and Hyalomma impeltatum. A total of 126 partially engorged adult ticks, collected from 40 animals, were screened for the presence of rickettsial DNA by conventional PCR targeting the ompB gene, followed by ompA and gltA targets and bidirectional sequencing. As a result of the sequence analyses, that at least three different species of pathogenic spotted fever group rickettsiae were detected. Rickettsia parkeri-like was detected in a R. sanguineus s.l. (n=1) collected from an African wildcat from Morocco. Rickettsia aeschlimannii was detected in a H. impeltatum (n=1) collected from a gerbil rodent. Rickettsia massiliae was detected in R. sanguineus s.l. ticks (n=5) collected from two Ruppells' foxes. The herein study demonstrates that pathogenic Rickettsia species are circulating in Morocco and Mauritania wildlife.

North African fox genomes show signatures of repeated introgression and adaptation to life in deserts.

Elucidating the evolutionary process of animal adaptation to deserts is key to understanding adaptive responses to climate change. Here we generated 82 individual whole genomes of four fox species (genus Vulpes) inhabiting the Sahara Desert at different evolutionary times. We show that adaptation of new colonizing species to a hot arid environment has probably been facilitated by introgression and trans-species polymorphisms shared with older desert resident species, including a putatively adaptive 25 Mb genomic region. Scans for signatures of selection implicated genes affecting temperature perception, non-renal water loss and heat production in the recent adaptation of North African red foxes (Vulpes vulpes), after divergence from Eurasian populations approximately 78 thousand years ago. In the extreme desert specialists, Rueppell's fox (V. rueppellii) and fennec (V. zerda), we identified repeated signatures of selection in genes affecting renal water homeostasis supported by gene expression and physiological differences. Our study provides insights into the mechanisms and genetic underpinnings of a natural experiment of repeated adaptation to extreme conditions.

Variation of Rodents' Body Temperature across Elevation in Alps.

AbstractUnderstanding the physiological adaptations of animals living in mountain landscapes is a key to predicting the responses of individuals to environmental changes, especially those imposed by climate. In this regard, the mechanism of body temperature regulation is particularly important in determining the physiological limits for activity under hypoxic and climatic stressful conditions. Numerous studies have shown that body temperature of rodents and other animals decreases with elevation and with extreme winter temperatures. But surprisingly, it is still not known how body temperature of wild animals varies along elevation during their reproductive seasons. We studied variation in core body temperature among individuals (N=294) of four rodent species (Apodemus flavicollis, Apodemus sylvaticus, Apodemus alpicola, Myodes glareolus) and its association with elevation (from 400 to 1,822 m asl), accounting for variation in environment temperature, microhabitat structure, body condition, and sex. Results showed a strong positive effect of elevation and a more limited effect of environmental temperature on rodents' body temperature during spring and summer. The effect of elevation on body temperature was influenced neither by interactions with environmental temperature or sex nor by the microhabitat structure. We suggest that in normothermic condition at high elevations, small mammals experiencing hypoxic exposure might show physiological adjustments for increasing efficiency of thermoregulation in low oxygen conditions.

Diversity, distribution and conservation of land mammals in Mauritania, North-West Africa.

Detailed knowledge about biodiversity distribution is critical for monitoring the biological effects of global change processes. Biodiversity knowledge gaps hamper the monitoring of conservation trends and they are especially evident in the desert biome. Mauritania constitutes a remarkable example on how remoteness and regional insecurity affect current knowledge gaps. Mammals remain one of the least studied groups in this country, without a concerted species checklist, the mapping of regions concentrating mammal diversity, or a national assessment of their conservation status. This work assessed the diversity, distribution, and conservation of land mammals in Mauritania. A total of 6,718 published and original observations were assembled in a spatial database and used to update the occurrence status, distribution area, and conservation status. The updated taxonomic list comprises 107 species, including 93 extant, 12 Regionally Extinct, and 2 Extinct in the Wild. Mapping of species distributions allowed locating concentrations of extant mammal species richness in coastal areas, along the Senegal River valley, and in mountain plateaus. Recent regional extinction of large-sized Artiodactyla and Carnivora has been very high (11% extinct species). From the extant mammals, 11% are threatened, including flagship species (e.g., Addax nasomaculatus and Panthera pardus). Species richness is poorly represented by the current protected areas. Despite the strong advances made, 23% of species categorise as Data Deficient. Persisting systematics and distribution uncertainties require further research. Field surveys in currently unexplored areas (northern and south-eastern regions) are urgently needed to increase knowledge about threatened mammals. The long-term conservation of land mammals in Mauritania is embedded in a complex web of socioeconomic and environmental factors that call for collaborative action and investment in sustainable human development. The current work sets the baseline for the future development of detailed research studies and to address the general challenges faced by mammals and biodiversity in the country.

Interpretation of gut microbiota data in the 'eye of the beholder': A commentary and re-evaluation of data from 'Impacts of radiation exposure on the bacterial and fungal microbiome of small mammals in the Chernobyl Exclusion Zone'.

Evidence that exposure to environmental pollutants can alter the gut microbiota composition of wildlife includes studies of rodents exposed to radionuclides. Antwis et al. (2021) used amplicon sequencing to characterise the gut microbiota of four species of rodent (Myodes glareolus, Apodemus agrarius, A. flavicollis and A. sylvaticus) inhabiting the Chernobyl Exclusion Zone (CEZ) to examine possible changes in gut bacteria (microbiota) and gut fungi (mycobiota) associated with exposure to radionuclides and whether the sample type (from caecum or faeces) affected the analysis. The conclusions derived from the analyses of gut mycobiota are based on data that represent a mixture of ingested fungi (e.g. edible macrofungi, polypores, lichens and ectomycorrhizae) and gut mycobiota (e.g. microfungi and yeasts), which mask the patterns of inter- and intraspecific variation in the authentic gut mycobiota. Implying that 'faecal samples are not an accurate indicator of gut composition' creates an unnecessary controversy about faecal sampling because the comparison of samples from the caecum and faeces confounds many other possible drivers (including different animals from different locations, sampled in different years) of variation in gut microbiota. It is relevant also that Antwis et al.'s (2021) data lack statistical power to detect an effect of exposure to radionuclides on the gut microbiota because (1) all of their samples of Apodemus mice had experienced a medium or high total absorbed dose rate and (2) they did not collect samples of bank voles (M. glareolus) from replicate contaminated and uncontaminated locations. Discussion of Antwis et al.'s (2021) analysis, especially the claims presented in the Abstract, is important to prevent controversy about the outcome of research on the biological impacts of wildlife inhabiting the CEZ.

Energetic dissociation of individual and species ranges.

The use of energy is universal to all life forms and all levels of biological organization, potentially linking processes operating at variable scales. Individual and species ranges might be energetically constrained, yet divergent metabolic limitations at both scales can disassociate these individual and species traits. We analysed comparative energetic and range data to unravel the mechanistic basis of the dissociation between individual and species range sizes observed among mammalian species. Our results demonstrate that basal, or maintenance, metabolism negatively correlates with individual ranges, but, at the same time, it positively correlates with species ranges. High aerobic capacity, i.e. maximum metabolic rate, positively correlates with individual ranges, but it is weakly related to species range size. These antagonistic energetic constraints on both ranges could lead to a disassociation between individual and species traits and to a low covariation between home and species range sizes. We show that important organismal functions, such as basal and maximum metabolic rates, have the potential to unravel mechanisms operating at different levels of biological organization and to expose links between energy-dependent processes at different scales.

Individual quality and phenology mediate the effect of radioactive contamination on body temperature in Chernobyl barn swallows.

Anthropogenic stressors, such as radioactive contaminants released from the Chernobyl and Fukushima Daiichi accidents, deteriorate ecological and evolutionary processes, as evidence for damaging effects of radioactive contamination on wildlife is accumulating. Yet little is known about physiological traits of animals inhabiting contaminated areas, and how those are affected by individual quality and phenology. We investigated variation in body temperature of wild barn swallows, Hirundo rustica, exposed to radioactive contamination from the Chernobyl accident in Ukraine and Belarus. We tested whether exposure to variable levels of radioactive contamination modified core body temperature of birds, and whether individual and phenological characteristics modulated radiosensitivity of body temperature. We showed that barn swallow body temperature varied with exposure to environmental radioactive contamination and that individual characteristics and phenology affected radioactive exposure. Increased radiosensitivity and up-regulation of body temperature were detected in birds of low body condition, high risk of capture, and in animals captured late during the day but early during the season. These results highlight the complex ways that the body temperature of a wild bird is impacted by exposure to increased radioactive contamination in natural habitats. By impacting body temperature, increased radioactive contamination may compromise energetic balance, jeopardize responsiveness to global warming, and increase risk of overheating.

Comparable response of wild rodent gut microbiome to anthropogenic habitat contamination.

Species identity is thought to dominate over environment in shaping wild rodent gut microbiota, but it remains unknown whether the responses of host gut microbiota to shared anthropogenic habitat impacts are species-specific or if the general gut microbiota response is similar across host species. Here, we compare the influence of exposure to radionuclide contamination on the gut microbiota of four wild mouse species: Apodemus flavicollis, A. sylvaticus, A. speciosus and A. argenteus. Building on the evidence that radiation impacts bank vole (Myodes glareolus) gut microbiota, we hypothesized that radiation exposure has a general impact on rodent gut microbiota. Because we sampled (n = 288) two species pairs of Apodemus mice that occur in sympatry in habitats affected by the Chernobyl and Fukushima nuclear accidents, these comparisons provide an opportunity for a general assessment of the effects of exposure to environmental contamination (radionuclides) on gut microbiota across host phylogeny and geographical areas. In general agreement with our hypothesis, analyses of bacterial 16S rRNA gene sequences revealed that radiation exposure alters the gut microbiota composition and structure in three of the four species of Apodemus mice. The notable lack of an association between the gut microbiota and soil radionuclide contamination in one mouse species from Fukushima (A. argenteus) probably reflects host "radiation escape" through its unique tree-dwelling lifestyle. The finding that host ecology can modulate effects of radiation exposure offers an interesting counterpoint for future analyses into effects of radiation or any other toxic exposure on host and its associated microbiota. Our data show that exposure to radionuclide contamination is linked to comparable gut microbiota responses across multiple species of rodents.

Energetic constraints on mammalian distribution areas.

Energy is a universal resource essential for all life functions. The rate of transformation of energy into an organism, and the energetic investment into reproduction, determines population and ecological-level processes. Several hypotheses predicted that the ecological expansion and size of the geographic distribution of a species are shaped by, among other factors, metabolic performance. However, how organismal energetic characteristics contribute to species geographic range size is poorly understood. With phylogenetic comparative methods whether energetic maintenance costs (basal metabolic rate, BMR), aerobic capacity (maximum exercise metabolic rate, VO2 max), summit thermoregulation (summit metabolic rate, VO2 sum) and the ability to sustain energy provisioning (daily energy expenditure, DEE) determine the distribution of mammalian species range sizes was tested. Both basal and maximum exercise metabolic rates (accounting for body mass), but not summit thermogenic metabolic rate, were positively associated with species range sizes. Furthermore, daily energy expenditure (accounting for body mass) was positively associated with species ranges. Body mass (accounting for energetic maintenance) was negatively related to range sizes. High aerobic exercise capacity, aiding mobility such as running and dispersal, and high sustained energy provisioning, aiding reproductive effort such as pregnancy, lactation and natal dispersal, can facilitate the establishment of large mammalian geographic ranges. Consequently, the pace of organismal physiological processes can shape important ecological and biodiversity patterns by setting limits to species' range sizes.

Applying the Anna Karenina principle for wild animal gut microbiota: Temporal stability of the bank vole gut microbiota in a disturbed environment.

Gut microbiota play an important role in host health. Yet, the drivers and patterns of microbiota imbalance (dysbiosis) in wild animals remain largely unexplored. One hypothesised outcome of stress on animal microbiomes is a destabilised microbial community that is characterised by an increase in inter-individual differences compared with microbiomes of healthy animals, which are expected to be (a) temporally stable and (b) relatively similar among individuals. This set of predictions for response of microbiomes to stressors is known as the Anna Karenina principle (AKP) for animal microbiomes. We examine the AKP in a wild mammal inhabiting disturbed environments by conducting a capture-mark-recapture survey of bank voles Myodes glareolus in areas that contrast in levels of radionuclide contamination (Chernobyl, Ukraine). Counter to key predictions of the AKP, bank voles that are not exposed to radionuclides harbour variable (increased inter-individual differences) and temporally dynamic gut microbiota communities, presumably tracking the natural spatio-temporal variation in resources. Conversely, bank voles exposed to radionuclides host more similar gut microbiota communities that are temporally stable, potentially due to a dysbiosis or selection (on host or bacteria) imposed by chronic radiation exposure. The implication of these data is that environmental stress (radiation exposure) can constrain the natural spatial and temporal variation of wild animal gut microbiota.

The effect of chronic low-dose environmental radiation on organ mass of bank voles in the Chernobyl exclusion zone.

PURPOSE: Animals are exposed to environmental ionizing radiation (IR) externally through proximity to contaminated soil and internally through ingestion and inhalation of radionuclides. Internal organs can respond to radioactive contamination through physiological stress. Chronic stress can compromise the size of physiologically active organs, but studies on wild mammal populations are scarce. The effects of environmental IR contamination on organ masses were studied by using a wild rodent inhabiting the Chernobyl exclusion zone (CEZ). MATERIAL AND METHODS: The masses of brain, heart, kidney, spleen, liver and lung were assessed from bank voles (Myodes glareolus) captured from areas across radioactive contamination gradient within the CEZ. Relative organ masses were used to correct for the body mass of an individual. RESULTS: Results showed a significant negative correlation between IR level in the environment and relative brain and kidney mass. A significant positive correlation between IR and relative heart mass was also found. Principal component analysis (PCA) also suggested positive relationship between IR and relative spleen mass; however, this relationship was not significant when spleen was analyzed separately. There was no apparent relationship between IR and relative liver or lung mass. CONCLUSIONS: Results suggest that in the wild populations even low but chronic doses of IR can lead to changes in relative organ mass. The novelty of these result is showing that exposure to low doses can affect the organ masses in similar fashion as previously shown on high, acute, radiation doses. These data support the hypothesis that wildlife might be more sensitive to IR than animals used in laboratory studies. However, more research is needed to rule out the other indirect effects such as radiosensitivity of the food sources or possible combined stress effects from e.g. infections.

The metabolic performance predicts home range size of bank voles: a support for the behavioral-bioenergetics theory.

The pace-of-life syndrome describes covariation between life-history, behavioral and physiological traits; while, the emerging behavioral-bioenergetics theory proposes mechanistic links between those traits in a spatial-ecological context. However, little is known about the association between the limits to metabolic rate and spatial performance (i.e., mobility, home range size) in free-living individuals. Here we show, for the first time at the intra-specific level, that mobility traits increased with the aerobic exercise capacity ([Formula: see text]O2max) in a wild rodent, the bank vole (Myodes glareolus): [Formula: see text]O2max affected directly the movement intensity, which in turn affected home ranges. The results show that evolution of high [Formula: see text]O2max could be driven by selection for spatial performance traits, and corroborate one of the key assumptions of the behavioral-bioenergetics theory. However, the minimum maintenance metabolism, measured as the basal metabolic rate (BMR), was not correlated with movement intensity, and the direction of the BMR-home range correlation tended to change with age of the voles. The latter result indicates that testing the theory will be particularly challenging.

Camouflage accuracy in Sahara-Sahel desert rodents.

Camouflage helps animals to hide from predators and is therefore key to survival. Although widespread convergence of animal phenotypes to their natural environment is well-established, there is a lack of knowledge about how species compromise camouflage accuracy across different background types in their habitat. Here we tested how background matching has responded to top-down selection by avian and mammalian predators using Sahara-Sahel desert rodents in North Africa. We show that the fur colouration of several species has become an accurate match to different types of desert habitats. This is supported by a correlation analysis of colour and pattern metrics, investigation of animal-to-background similarities at different spatial scales and is confirmed by modelling of two predator vision systems. The background match was closest across large (or global) spatial scales, suggesting a generalist camouflage tactic for many background types. Some species, may have a better match to the background over small (or focal) spatial scales, which could be the result of habitat choices or differential predation. Nevertheless, predicted discrimination distances of fur colouration were virtually indistinguishable for mammalian and low for avian vision model, which implies effective camouflage. Our study provides one of the best documented cases of multilevel camouflage accuracy in geographically widespread taxa. We conclude that background matching has become an effective and common adaptation against predatory threat in Sahara-Sahelian desert rodents.

Evolutionary history of two cryptic species of northern African jerboas.

BACKGROUND: Climatic variation and geologic change both play significant roles in shaping species distributions, thus affecting their evolutionary history. In Sahara-Sahel, climatic oscillations shifted the desert extent during the Pliocene-Pleistocene interval, triggering the diversification of several species. Here, we investigated how these biogeographical and ecological events have shaped patterns of genetic diversity and divergence in African Jerboas, desert specialist rodents. We focused on two sister and cryptic species, Jaculus jaculus and J. hirtipes, where we (1) evaluated their genetic differentiation, (2) reconstructed their evolutionary and demographic history; (3) tested the level of gene flow between them, and (4) assessed their ecological niche divergence. RESULTS: The analyses based on 231 individuals sampled throughout North Africa, 8 sequence fragments (one mitochondrial and seven single copy nuclear DNA, including two candidate genes for fur coloration: MC1R and Agouti), 6 microsatellite markers and ecological modelling revealed: (1) two distinct genetic lineages with overlapping distributions, in agreement with their classification as different species, J. jaculus and J. hirtipes, with (2) low levels of gene flow and strong species divergence, (3) high haplotypic diversity without evident geographic structure within species, and (4) a low level of large-scale ecological divergence between the two taxa, suggesting species micro-habitat specialization. CONCLUSIONS: Overall, our results suggest a speciation event that occurred during the Pliocene-Pleistocene transition. The contemporary distribution of genetic variation suggests ongoing population expansions. Despite the largely overlapping distributions at a macrogeographic scale, our genetic results suggest that the two species remain reproductively isolated, as only negligible levels of gene flow were observed. The overlapping ecological preferences at a macro-geographic scale and the ecological divergence at the micro-habitat scale suggest that local adaptation may have played a crucial role in the speciation process of these species.

Exposure to environmental radionuclides associates with tissue-specific impacts on telomerase expression and telomere length.

Telomeres, the protective structures at the ends of chromosomes, can be shortened when individuals are exposed to stress. In some species, the enzyme telomerase is expressed in adult somatic tissues, and potentially protects or lengthens telomeres. Telomeres can be damaged by ionizing radiation and oxidative stress, although the effect of chronic exposure to elevated levels of radiation on telomere maintenance is unknown for natural populations. We quantified telomerase expression and telomere length (TL) in different tissues of the bank vole Myodes glareolus, collected from the Chernobyl Exclusion Zone, an environment heterogeneously contaminated with radionuclides, and from uncontaminated control sites elsewhere in Ukraine. Inhabiting the Chernobyl Exclusion Zone was associated with reduced TL in the liver and testis, and upregulation of telomerase in brain and liver. Thus upregulation of telomerase does not appear to associate with longer telomeres but may reflect protective functions other than telomere maintenance or an attempt to maintain shorter telomeres in a stressful environment. Tissue specific differences in the rate of telomere attrition and apparent radiosensitivity weaken the intra-individual correlation in telomere length among tissues in voles exposed to radionuclides. Our data show that ionizing radiation alters telomere homeostasis in wild animal populations in tissue specific ways.

Repeated evolution of camouflage in speciose desert rodents.

There are two main factors explaining variation among species and the evolution of characters along phylogeny: adaptive change, including phenotypic and genetic responses to selective pressures, and phylogenetic inertia, or the resemblance between species due to shared phylogenetic history. Phenotype-habitat colour match, a classic Darwinian example of the evolution of camouflage (crypsis), offers the opportunity to test the importance of historical versus ecological mechanisms in shaping phenotypes among phylogenetically closely related taxa. To assess it, we investigated fur (phenotypic data) and habitat (remote sensing data) colourations, along with phylogenetic information, in the species-rich Gerbillus genus. Overall, we found a strong phenotype-habitat match, once the phylogenetic signal is taken into account. We found that camouflage has been acquired and lost repeatedly in the course of the evolutionary history of Gerbillus. Our results suggest that fur colouration and its covariation with habitat is a relatively labile character in mammals, potentially responding quickly to selection. Relatively unconstrained and substantial genetic basis, as well as structural and functional independence from other fitness traits of mammalian colouration might be responsible for that observation.