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Despite the presence of mostly endemic species, the most comprehensive data set on the distribution and ecology of small mammals inhabiting Simien Mountains National Park (SMNP) dated from 1927. The study we carried out and report here provides a unique opportunity to assess the possible role of climate change over the last 88 years on the elevational distribution of mammals in the Ethiopian highlands. Between September and November 2015, three of us (EWC, WTS, YM) collected nonvolant small mammals at four sites (2,900, 3,250, 3,600, and 4,000 m a.s.l.) along the western slope of the Simien Mountains using standardized sampling. Over a 4-week period we recorded 13 species, comprising 11 species of rodents and two of shrews, all endemic to the Ethiopian Plateau. We found the greatest species richness at mid-elevations (3,250 m), consistent with a general pattern found on many other mountains worldwide, but less so in Africa. We compared our species distribution results to the 1927 data set and found upward elevational shifts in species' ranges, highlighting the role and influence of climate change on the small mammal community. SMNP represents an exceptionally valuable core area of endemism and the best protected natural habitat in northern Ethiopia.
Mammalian spatial and temporal activity patterns can vary depending on foraging behavior or the perception of predation or competition risk among species. These behaviors may in turn be altered by human influences such as defaunation. Herein, we evaluate whether frugivores avoid areas with high visitation rates by potential predators or competitors, and whether this avoidance changes in areas with different degrees of defaunation. We installed 189 cameras under fruit trees in six areas of the Atlantic Forest, Brazil, that differ in the abundance of top predators and large frugivores. Small predators and small frugivores were more frequent at night while large frugivores were more frequent during the day, but small frugivores visited and spent less time at fruiting trees on brighter nights, unlike large predators and large frugivores. Small frugivores also were less frequent in areas with high visitation by large frugivores and more frequent in highly defaunated areas. Our results suggest that the dynamics among mammalian functional groups varied according to diel patterns, potential competitors, and defaunation. We highlight the importance of understanding how species interactions are changing in areas exposed to strong human impacts to mitigate the indirect effects of defaunation.
We evaluated the response of a remnant population of yellow-bellied marmots (Marmota flaviventris) to targeted habitat enhancement in an ecological system that had been degraded during ∼100 years of intensive livestock management, including marmot eradication. We used capture-recapture data and a novel use of a multistate framework to evaluate geographic expansion of the marmot population pre- and post-habitat enhancement. We also estimated age-structured survival, reproduction, and sex ratios. The marmot population appeared to respond positively to new habitat opportunities created by habitat enhancement: the number of marmots captured increased from three marmots pre-habitat enhancement to 54 (28 adults and yearlings, 26 young) post-habitat enhancement at the end of the study. Marmots expanded geographically by transitioning into habitat-enhanced areas, and adult females occupied and reproduced in all habitat-enhanced areas. The sex ratio of the young population in 2019 was strongly female-biased, which may have been influenced by poor body condition of breeding females owing to unusually prolonged snow cover that year. Adult and yearling survival were within the range of that reported for colonial adults and yearlings in Colorado. Our results suggest that active habitat enhancement can assist in the recovery of marmot populations in systems where marmots historically existed.
Research on sociality in temperate ground-dwelling squirrels has focused on female philopatry and other life history trade-offs, which are influenced by constraints in the duration of the active growing season. Temperate ground-dwelling squirrels that experience high predation pressure, are large in body size, and have a short active season, show a more complex social organization. In contrast, African ground squirrels are active year-round, suggesting that instead of a short active season, distinct selective pressures influence their social organization. We examined the social organization of Barbary ground squirrels, Atlantoxerus getulus, and compared the social organization of temperate and African ground-dwelling sciurids. Anecdotal accounts on Barbary ground squirrels' social organization suggested that they were either solitary or gregarious, or live in small family groups. We recorded the group size, composition, cohesion, and genetic relatedness, of the population on the arid island of Fuerteventura, Spain. Our data indicate that females live in small (1–8) all-female kin groups separate from adult males, and that unrelated adult males share sleeping burrows with immature individuals of either sex. We observed sex-biased dispersal with males primarily the dispersing sex and females primarily philopatric. Females sleep solitarily during gestation and lactation and nest either communally or singly after juvenile emergence. During the day, males and females can be active in the same area. Barbary ground squirrels are social because the squirrels share sleeping burrows and show spatiotemporal overlap. Barbary ground squirrels' social organization resembles that of the closely related Cape ground squirrel rather than that of the temperate ground-dwelling sciurids, although the former are more temperate, seasonal breeders. In addition to describing the social organization of a previously unstudied species, this paper sheds light on the ecological drivers of sociality, and the evolution of distinct social organizations in ground-dwelling sciurids.
Swift foxes (Vulpes velox) are endemic to the Great Plains of North America, but were extirpated from the northern portion of their range by the mid-1900s. Despite several reintroductions to the Northern Great Plains, there remains a ∼350 km range gap between the swift fox population along the Montana and Canada border and that in northeastern Wyoming and northwestern South Dakota. A better understanding of what resources swift foxes use along the Montana and Canada border region will assist managers to facilitate connectivity among populations. From 2016 to 2018, we estimated the home range size and evaluated resource use within the home ranges of 22 swift foxes equipped with Global Positioning System tracking collars in northeastern Montana. Swift fox home ranges in our study were some of the largest ever recorded, averaging (± SE) 42.0 km2 ± 4.7. Our results indicate that both environmental and anthropogenic factors influenced resource use. At the population level, resource use increased by 3.3% for every 5.0% increase in percent grasslands. Relative probability of use decreased by 7.9% and 7.4% for every kilometer away from unpaved roads and gas well sites, respectively, and decreased by 3.0% and 11.3% for every one-unit increase in topographic roughness and every 0.05 increase in normalized difference vegetation index (NDVI), respectively. Our study suggests that, to reestablish connectivity among swift fox populations in Montana, managers should aim to maintain large corridors of contiguous grasslands at a landscape scale, a process that likely will require having to work with multiple property owners.
In tropical forests, the diets of many frugivorous mammals overlap, yet how hyper-diverse assemblages of consumers exploit resources and coexist remains poorly understood. We evaluated competitive interactions among three species of terrestrial frugivorous mammals, the ungulate Tayassu pecari (white-lipped peccary), its close relative Pecari tajacu (collared peccary), and a large rodent (Dasyprocta azarae, agouti), in their exploitation strategies of palm resources of different quality. We conducted the study in a large isolated fragment at the tropical Atlantic Forest of Brazil, where these mammal species show high spatial and temporal overlap. We evaluated if body mass and foraging group size define a hierarchy in exploitation of preferentially richer palm resources. We used camera traps and two-species occupancy models to examine patterns of co-occurrence and variable interaction strength between these consumers and three species of palms. Our analyses supported the hypothesis of partial resource overlap but no competition among frugivores, and a body mass dominance hierarchical exploitation of resources. The larger frugivore (white-lipped peccary) dominated patches of the lipid-rich palm Euterpe edulis, where the smallest frugivore (agouti) was absent. Instead, the smallest frugivore concentrated its foraging in areas with the poorest palm resource, Syagrus oleracea. Collared peccaries preferred areas of high abundance of Syagrus romanzoffiana when the other two mammal species were rarely detected or absent, strongly avoided patches of E. edulis, and showed higher average detection probabilities when agoutis were present. Our study highlights the important role of behavioral plasticity in promoting coexistence and indicates that through context-dependent interactions and hierarchical partitioning of resources, consumers can avoid strong competition, even under conditions of high spatial and temporal overlap and high levels of habitat fragmentation and isolation.
Heterospecific competitors can use chemical cues left by dominant species to avoid aggressive interactions. Similarly, prey avoid chemical cues from predators at feeding sites, presumably because risk of death outweighs the benefit of food. This study addressed the lack of information regarding mammals' avoidance of direct cues from competitors and also examined how indirect cues, i.e., vegetative cover, affect foraging behavior. To test if chemical cues and vegetative cover alter the number of visits by prey species and time spent at feeding plots, we observed snowshoe hares (Lepus americanus) in plots containing coyote (Canis latrans; predator) and moose (Alces alces; competitor) urine across a spectrum of vegetation densities. Snowshoe hares significantly reduced number of visits to plots that contained coyote or moose urine. In plots treated with coyote urine, number of visits decreased significantly as plots became more densely vegetated. Neither chemical cues nor vegetation density affected time spent in plots. These results suggest that competition between snowshoe hares and moose has selected for an avoidance response. This study also reinforces the idea that an increase in vegetation density could prove disadvantageous to prey, perhaps because some predators use dense vegetation to their advantage.
Capybaras, Hydrochoerus hydrochaeris (Rodentia: Caviidae: Hydrochoerinae), show a strict social hierarchy among males, wherein the top-ranking male gains preferential access to females. Despite minimal sexual size dimorphism, males have a prominent scent gland on their snouts that is greatly reduced in the females. Top-ranking males have a larger gland and mark more frequently than subordinate males. This species also shows a moderately complex courtship that seems to be modulated by female behavior. In this study, we evaluated several components of courtship, as well as the females' interactions with males during and outside courtship, in relation to the hierarchy rank of males. We found that subordinate males engaged in longer courtships than top-ranking males. However, there was no difference in the number of mount attempts or the success rate of these mounts as a function of the social status of the male, despite the longer courtship performed by subordinate males in comparison to top-ranking males. Outside courtship, females directed the same number of social interactions to males regardless of status. However, during courtship, females avoided copulation by subordinate males both directly and indirectly by encouraging courtship disruption by higher-ranking males. Females' avoidance of subordinates may force these males to invest a higher amount of effort in courtships, thus engaging in longer courtships, yet achieving similar mount success as top-ranking males. We show that the original assumption of male hierarchy as the main mechanism of reproductive distribution is incomplete, and female mate choice plays an important role in determining which males reproduce.
Habitat structure may have a significant influence on the occurrence, abundance, and activity patterns of forest mammals. However, anthropogenic habitat disturbance changes habitat structure, which may alter those patterns of activity. We assessed occurrence, relative abundance, and activity patterns of Dromiciops gliroides, an arboreal marsupial endemic to the temperate rainforests of southern South America, contrasting four forest conditions at a regional scale: old-growth, second-growth, and logged forests, and abandoned exotic plantations. We conducted a camera-trap assessment in two consecutive austral summers across most of the Chilean range of D. gliroides, and compared habitat structure along a disturbance gradient. All structural features assessed differed among forest conditions. Dromiciops gliroides was present in all forest conditions, but its abundance decreased and activity got narrower as disturbance increased, being significantly lower in the exotic plantations. Activity patterns were variable among forest conditions and months, and were significantly more restricted temporally at exotic plantations. Although D. gliroides is tolerant to habitat disturbance, we show that structural alteration results in lower abundances and narrower activity patterns.
Understanding variability in growth patterns of marine mammals provides insights into the health of individuals and status of populations. Body growth of gray whales (Eschrichtius robustus) has been described for particular life stages, but has not been quantified across all ages. We derived a comprehensive growth equation for gray whales by fitting a two-phased growth model to age-specific length data of eastern North Pacific gray whales that were captured, stranded, or harvested between 1926 and 1997. To predict mass-at-age, we used the allometric relationship between mass and length. We found that on average (± SD), calves were 4.6 ± 0.043 m and 972 ± 26 kg at birth, and reached 8.5 ± 0.095 m and 6,019 ± 196 kg by the end of their first year of life (n = 118). Thus, calves almost double (2×) in length and octuple (8×) in mass while nursing, and are effectively about two-thirds of their asymptotic adult length and one-third of their maximum mass when weaned. The large sample of aged individuals (n = 730) indicates that gray whales live up to ∼48 years and have a life expectancy of < 30 years. Adult females attain a mean (± SD) asymptotic size of 13.1 ± 0.048 m and 20,758 ± 222 kg, while the smaller males average 12.6 ± 0.048 m and 19,938 ± 222 kg at ∼40 years of age. Females are thereby ∼4% longer and heavier than males. These age-specific estimates of body size can be used to estimate food requirements and assess nutritional status of individuals.
William S. Beatty, Patrick R. Lemons, Suresh A. Sethi, Jason P. Everett, Cara J. Lewis, Robert J. Lynn, Geoffrey M. Cook, Joel L. Garlich-Miller, John K. Wenburg
The kin structure of a species at relatively fine spatial scales impacts broad-scale patterns in genetic structure at the population level. However, kin structure rarely has been elucidated for migratory marine mammals. The Pacific walrus (Odobenus rosmarus divergens) exhibits migratory behavior linked to seasonal patterns in sea ice dynamics. Consequently, information on the spatial genetic structure of the subspecies, including kin structure, could aid wildlife managers in designing future studies to evaluate the impacts of sea ice loss on the subspecies. We sampled 8,303 individual walruses over a 5-year period and used 114 single-nucleotide polymorphisms to examine both broad-scale patterns in genetic structure and fine-scale patterns in relatedness. We did not detect any evidence of genetic structure at broad spatial scales, with low FST values (≤ 0.001) across all pairs of putative aggregations. To evaluate kin structure at fine spatial scales, we defined a walrus group as a cluster of resting individuals that were less than one walrus body length apart. We found weak evidence of kin structure at fine spatial scales, with 3.72% of groups exhibiting mean relatedness values greater than expected by chance, and a significantly higher overall observed mean value of relatedness within groups than expected by chance. Thus, the high spatiotemporal variation in the distribution of resources in the Pacific Arctic environment likely has favored a gregarious social system in Pacific walruses, with unrelated animals forming temporary associations.
Carnivores are decreasing globally due in part to anthropogenic ecological disturbances. In Argentina, human activities have fragmented wildlife habitat, thereby intensifying puma–livestock conflict and leading to population control of the predator species by hunting. We investigated genetic variability and population structure of pumas (Puma concolor) from three south-central Argentine provinces with two different management policies for the species: full protection versus legal hunting. All genetic estimates were based on 83 individuals genotyped at 25 species-specific microsatellite loci. The overall genetic diversity was high (observed heterozygosity = 0.63), but lower than in other South American populations. Spatial analyses revealed the presence of two bottlenecked genetic clusters with very similar diversity and low gene flow (3% per generation) between them. However, analyses based on a priori separated groups showed that gene flow follows increasing values of hunting pressure, converging to the area with the greatest number of individuals harvested. Our results suggest that hunting pressure likely is contributing to the gene flow pattern, limiting pumas' movements and creating a metapopulation dynamic among geographic subpopulations. Integrated demographic and genetic approaches are needed to better understand pumas' movements across the landscape and adopt successful management plans to achieve long-term population viability.
Emerging infectious diseases have recently increased in wildlife and can result in population declines and the loss of genetic diversity in susceptible populations. As populations of impacted species decline, genetic diversity can be lost, with ramifications including reduced effective population size and increased population structuring. For species of conservation concern, which may already have low genetic diversity, the loss of genetic diversity can be especially important. To investigate the impacts of a novel pathogen on genetic diversity in a genetically depauperate endangered species, we assessed the ramifications of a sylvatic plague-induced bottleneck in black-footed ferrets (Mustela nigripes). Following a plague epizootic, we genotyped 184 ferrets from Conata Basin and Badlands National Park, South Dakota, at seven microsatellite loci. We compared our results to pre-plague studies in the same population. We observed population substructuring into three genetic clusters. These clusters reflect founder effects from ferret reintroduction events followed by genetic drift. Compared to the pre-plague population, we observed losses of allelic diversity in all clusters, as well as significantly reduced heterozygosity in one cluster. These results indicate that disease epizootics may reduce population size and also genetic diversity. Our results suggest the importance of early and sustained management in mitigating disease epizootics in naïve populations for the maintenance of genetic diversity.
Climate change can have particularly severe consequences for high-elevation species that are well-adapted to long-lasting snow conditions within their habitats. One such species is the wolverine, Gulo gulo, with several studies showing a strong, year-round association of the species with the area defined by persistent spring snow cover. This bioclimatic niche also predicts successful dispersal paths for wolverines in the contiguous United States, where the species shows low levels of genetic exchange and low effective population size. Here, we assess the influence of additional climatic, vegetative, topographic, and anthropogenic, variables on wolverine genetic structure in this region using a multivariate, multiscale, landscape genetic approach. This approach allows us to detect landscape-genetic relationships both due to typical, small-scale genetic exchange within habitat, as well as exceptional, long-distance dispersal among habitats. Results suggest that a combination of snow depth, terrain ruggedness, and housing density, best predict gene flow in wolverines, and that the relative importance of variables is scale-dependent. Environmental variables (i.e., isolation-by-resistance, IBR) were responsible for 79% of the explained variation at small scales (i.e., up to ∼230 km), and 65% at broad scales (i.e., beyond ∼420 km). In contrast, a null model based on only space (i.e., isolation-by-distance, IBD) accounted only for 17% and 11% of the variation at small and broad scales, respectively. Snow depth was the most important variable for predicting genetic structures overall, and at small scales, where it contributed 43% to the variance explained. At broad spatial scales, housing density and terrain ruggedness were most important with contributions to explained variation of 55% and 25%, respectively. While the small-scale analysis most likely captures gene flow within typical wolverine habitat complexes, the broad-scale analysis reflects long-distance dispersal across areas not typically inhabited by wolverines. These findings help to refine our understanding of the processes shaping wolverine genetic structure, which is important for maintaining and improving functional connectivity among remaining wolverine populations.
Body size is an important trait in animals because it influences a multitude of additional life history traits. The causal mechanisms underlying body size patterns across spatial, temporal, and taxonomic hierarchies are debated, and of renewed interest in this era of climate change. Here, we tested multiple hypotheses regarding body mass patterns at the intraspecific and interspecific levels. We investigated body size patterns within a climate-sensitive small mammal species, Ochotona princeps (n = 2,873 individuals), across their range with local environmental variables. We also examined body mass of populations over time to determine if body size has evolved in situ in response to environmental change. At the interspecific level we compared the mean mass of 26 pika species (genus Ochotona) to determine if environmental temperatures, food availability, habitat variability, or range area influence body size. We found correlations between temperature, vegetation, and particularly precipitation variables, with body mass within O. princeps, but no linear relationship between body size and any climate or habitat variable for Ochotona species. Body size trends in relation to climate were stronger at the intraspecific than the interspecific level. Our results suggest that body size within O. princeps likely is related to food availability, and that body size evolution is not always a viable response to temperature change. Different mechanisms may be driving body size at the interspecific and intraspecific levels and factors other than environment, such as biotic interactions, may also be influential in determining body size over space and time.
The subfamily Dolichotinae (Rodentia, Caviidae) includes two living species (Dolichotis patagonum and D. salinicola) of cursorial, long-legged rodents that inhabit semiarid thorn scrubs and shrublands in southern South America. Some authors consider that the morphological differences between D. patagonum and D. salinicola warrant circumscription of the latter in its own genus, Pediolagus. Based on a phylogeny and divergence times grounded on molecular data, as well as a qualitative and quantitative assessment of morphological differences, the distinction between Dolichotis and Pediolagus is equal to or greater than differences seen for other intergeneric comparisons within Cavioidea. Based on these results, we argue that the taxonomic designations of Dolichotis and Pediolagus should be retained.
Akodontini, the second largest tribe within sigmodontine rodents, encompasses several stomach morphologies. This is striking because most sigmodontine groups of comparable taxonomic rank are very conservative in this respect. Based on extensive sampling of newly dissected specimens (213 stomachs representing 36 species), as well as published examples, covering almost all akodontine living genera (15 of 16), we undertook a reappraisal of the gross morphology of this organ. We then mapped this information, together with gallbladder occurrence, in a refined multilocus molecular phylogeny of the tribe. We surveyed three different configurations of stomachs in akodontines, according to the degree of development and location of the glandular epithelium; in addition, two minor variations of one of these types were described. Of the five major clades that integrate Akodontini, four are characterized by a single stomach morphology, while one clade exhibits two morphologies. Mapping stomach type on the phylogeny recovered two configurations for the most recent ancestor of Akodontini. A revised survey of gallbladder evidence also revealed overlooked congruencies. The observed stomach diversity and its arrangement in the phylogeny, along with additional morphological characters and the genetic diversity among the main clades, supports the necessity of changes in the current classification of the tribe. Recognition of subtribes or partitioning of Akodontini into several additional tribes of equal rank could be suitable options.
Neusticomys peruviensis is a poorly known sigmodontine rodent of the tribe Ichthyomyini, represented in collections by only five specimens collected in five localities from lowland forests of central and southern Peru. Recent expeditions in Llanchama, in northern Peru, north of the Río Amazonas, and near Allpahuayo Mishana Natural Reserve (Loreto, Peru), were successful in obtaining three specimens of Neusticomys. Based on morphological and meristic data, we found the population at Llanchama is distinct from the allopatric populations of N. peruviensis, and other species of Neusticomys. A species distribution model also shows the population at Llanchama is not highly predicted by the set of variables of the known localities of N. peruviensis. However, sequence data from the mitochondrial cytochrome-b gene indicate that genetic distinctiveness is low. Because intraspecific variability is important to understand evolutionary and biogeographic processes, and in concordance with the polytypic species concept, we interpret the population at Llanchama to represent a new subspecies of N. peruviensis that we describe in this paper.
Desert shrews of the genus Notiosorex comprise four species with morphological characteristics that are difficult to distinguish among the species. Indeed, N. cockrumi was described using only genetic markers. Based on molecular divergence documented in N. crawfordi, we hypothesize that a fifth species is present in the Baja California peninsula. Genetic variation at the species level was analyzed using individuals from locations west of the Colorado River in the Baja California peninsula, Mexico, and California, United States. Molecular markers of mitochondrial origin (cytochrome b, 1,140 bp; cytochrome c oxidase subunit I, 542 bp; and cytochrome c oxidase subunit III, 672 bp), as well as the nuclear intron 7 of the beta fibrinogen gene (385 bp) were used to construct a phylogeny for species of the genus Notiosorex. Genetic distances of 12.46–15.58% between west and east of the Colorado River were obtained using p-distance models. Our phylogenetic analyses showed almost identical topologies, placing populations from west of the Colorado River in three monophyletic clades with high bootstrap support values. Results of molecular phylogenetic identity among shrews of the genus Notiosorex support the existence of an undescribed, polytypic species of Notiosorex west of the Colorado River.
The peculiar sphenoidal “pits” of the common warthog (Phacochoerus africanus) long have been recognized as a feature that distinguishes that species from the closely related desert warthog (P. aethiopicus). Authors seem to regard these structures as blind pockets that do not extend beyond the basicranium. However, these structures actually are openings that lead into a complex system of sinuses (the sphenoidal sinuses) located in the sphenoid and squamosal, and occasionally extending into the occipital and parietal bones. The openings appear to serve as a drain into the nasopharynx. The sphenoidal “pits” of P. africanus as currently defined by most authors are, therefore, not homologous with the sphenoidal pits of P. aethiopicus. We suggest that the term “sphenoidal apertures” be applied to these openings. The true homologue of the sphenoidal pits of P. aethiopicus is the bone that surrounds the sphenoidal apertures in P. africanus. This would include the thin bony sheet that forms the floor of the opening and that bears a shallow fossa. We recommend the term “sphenoidal shelf” be employed to describe this part of the true sphenoidal pit of P. africanus. In addition to the sphenoidal sinuses, the maxillary and frontal sinuses of P. africanus also are described. We report the possibility of mammalian cranial sinuses arising from nasopharyngeal diverticula rather than from diverticula originating from the nasal cavity proper. Previously, such nasopharyngeal pneumatization only has been known to occur in Reptilia. Possible sinus functions are discussed including shock absorption, lightening of the skull, improvement of olfaction, and enhancement of the immune system. In addition to P. africanus, sphenoidal apertures also occur in Babyrousa, and in an extinct perissodactyl, a brontothere (= titanothere).
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