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The persistence of cold-adapted species along their equatorial range edge (i.e., southern range edge for species in the Northern Hemisphere and northern range edge for species in the Southern Hemisphere) is threatened by climate change. These species will be challenged not just by unfavorable climatic regimes, but also by changing biotic interactions, which may be more intense along equatorial edges. However, we currently have a poor understanding of the nature of biotic interactions at range edges and how climate may mediate those interactions, particularly for cold-adapted mammals. We studied the distribution of threatened Canada lynx (Lynx canadensis) at their southern range edge in northern Washington, United States from 2014 to 2016. Using data collected from 397 camera-trap stations in snow-on and snow-off seasons, and single- and 2-species occupancy models, we investigated seasonal patterns of habitat selection and spatial association of lynx with their primary prey (snowshoe hares, Lepus americanus) and potential competitors (bobcats, Lynx rufus; cougars, Puma concolor). Single-species occupancy models revealed lynx distribution was strongly associated with snowshoe hare abundance and topographic variables related to lower temperatures and increased moisture. In contrast, bobcats and cougars were more generalized in their habitat associations or displayed the reverse response to environmental variables. Spatial overlap of the 3 felid species increased during snow-off seasons. Two-species occupancy models showed a decrease in use of camera sites by lynx when bobcats were present, suggesting lynx were avoiding their warm-adapted competitor. Taken together, these results suggest that biotic interactions are partly shaping large-scale lynx distribution patterns along their southern range edge. Increasing temperatures and loss of snow may result in a combination of habitat isolation and potential for increased competitive interactions for lynx at the margins of their range.
Natural history collections have stimulated insights into systematics and evolution, but the extensive biodiversity sampling held in museums is increasingly employed to address other critical societal concerns, especially those related to changing environmental conditions on our planet. Due to large-scale digitization efforts in the last decade, specimen information can now be collated across natural history museums. Here, we leverage the availability of digital records of specimens in the United States that span the past ∼135 years to explore the vitality of this resource. Using mammals as an example, we document a significant decline in recent specimen acquisition at a time of extreme environmental degradation and loss of mammalian populations. To stimulate rigorous assessments of the impacts of changing conditions and future-proof this basic infrastructure for mammalogy, we recommend a renewed effort to build temporally deep, geographically extensive, and site-intensive collections of holistic specimens. Targeted fieldwork should be designed to leverage historic sampling to enable retrospective environmental analyses and derive more complete perspectives of change.
High-throughput sequencing methods have facilitated obtaining large amounts of data from degraded DNA, thus resulting in a dramatic increase in destructive sampling requests to museums. Because the tissues taken from museum specimens as sources of DNA are destroyed during analysis, consideration of the costs and benefits of loss of valuable specimen material relative to knowledge gained is required for any project utilizing destructive sampling. Variation exists in the preservation of DNA in historical specimens due to specimen age and type of museum preparation, among other factors. Thus, it is important to assess DNA yield and quality from different sources of museum specimens when considering the needs of a particular molecular project. We compared DNA derived from several common sources of museum specimens including bone, claw, skin, and soft tissue adherent to skeletal preparations. To account for differences in preparation type and therefore specimen preservation, we tested the performance of samples representing 3 taxonomic groups: mephitids, rodents, and marsupials. We also compared yields from 2 commonly used DNA extraction techniques. DNA quality was assessed by comparing average fragment size, concentration, and copy number of template DNA (for mitochondrial and nuclear markers) in genomic DNA extracts, as well as mitochondrial genome sequence coverage resulting from shotgun sequencing. We show that DNA quality derived from historic museum samples differs depending on specimen and sample type; however, all samples yielded high mitochondrial copy number except the skin and nail from the tanned specimen. Overall, claw samples produced the greatest number of high-quality sequencing reads with the least amount of bacterial contamination. We also found that high DNA concentrations did not necessarily result in high percentages of on-target reads; in fact, the samples that yielded the highest DNA quantities also had the highest amount of exogenous bacterial DNA. Our results indicate that most historical tissue types can be suitable for next-generation sequencing approaches, therefore providing multiple options for natural history collection staff and researchers when considering destructive sampling requests.
The long-recognized monotypic status of the relictual marsupial genus Dromiciops was recently challenged by a controversial reanalysis of previously published mtDNA data that were combined with a new morphological study to conclude that the genus contains 3 species: D. bozinovici, D. mondaca, and D. gliroides. We present here new phylogenetic and coalescent species delimitation analyses to test the multispecific status of Dromiciops relative to the proposed 3 new species. Our molecular analysis is based on partial sequences of 4 nuclear (RAG1, ApoB, vWF, and IRBP) and 2 mitochondrial (12S RNA and Cytb) genes. Genetic distances showed low differentiation among the proposed Dromiciops species, consistent with typical levels of intraspecific variation. Phylogenetic analyses yielded only moderate support for monophyly of D. bozinovici, while depicting polyphyly in D. gliroides and D. mondaca. Species delimitation analyses did not recover the proposed 3-species scenario, and the taxonomic index of congruence among these methods (Ctax = 0.5–1.0) supported monotypic status for Dromiciops. Taking into consideration all the genetic analyses and previously reported morphological analyses, we conclude that all Dromiciops lineages belong to a single species.
We describe a new species of squirrel (Sciuridae, Callosciurus) from Hon Khoai Island, located off the coast of southern Vietnam (centered at ca. 8°26′08″N, 104°49′58″E) and discuss its phylogenetic position in the genus Callosciurus. Compared to other Callosciurus occurring on the Indochina Peninsula, the new species (Callosciurus honkhoaiensis) is strikingly small, especially head and body length, body mass, and hind foot length. Unlike other species of Callosciurus, the hairs at the tip of the tail are white with a black base, and the venter and feet are whitish cream. The new species at present is known only from the type locality, Hon Khoai Island. Phylogenetically, the new species is closely related to C. caniceps, suggesting that it evolved from C. caniceps or an ancestor in common with C. caniceps, possibly during the Pliocene. Genetic distances between the 2 species calculated from comparison of mitochondrial cytochrome b sequences are 10.1–10.3%. During both glaciations and interglaciations of the Pleistocene, the new species may have been isolated from other Callosciurus populations by rivers and sea, respectively.
Nonbreeding season territoriality is found in many mammal species irrespective of diet, being found in carnivores, granivores, and herbivores. However, we know the hormonal basis for this behavior in virtually none. American martens (Martes americana) show strong intrasexual, year-round territoriality. We collected serum samples from both territorial and transient males and documented size metrics and movement patterns with live-capture and radiotelemetry from September to June in 3 years in Southeast Alaska. Dehydroepiandrosterone (DHEA—a prohormone that can be converted in the brain to active gonadal hormones) levels were high (comparable to humans and rodents showing nonbreeding season spacing behavior) and did not change over the nonbreeding season in territorial males. In contrast, testosterone levels were low in autumn and increased as the summer breeding season approached. Territorial males were larger than transients in some measures and had higher testosterone levels, but similar DHEA and cortisol levels (total and free). DHEA levels declined with age. Our evidence is consistent with the hypothesis that DHEA, not testosterone, is the basis for territoriality outside the breeding season in martens, but collection of serum from females and experimental manipulations are required to provide conclusive evidence.
Breeding strategies of cooperative breeders can vary widely ranging from multiple breeding pairs in a group, to polygamy, polyandry, and combinations of all 3 forms. Often, we do not have a clear understanding of the influences or mechanisms giving rise to the presence of multiple breeding individuals within groups. This is particularly true for animals that are difficult to manipulate or observe, such as large carnivores. I examined factors associated with the occurrence of multiple breeding individuals within groups in a population of recolonizing gray wolves (Canis lupus). Additionally, I investigated what might affect pup recruitment in groups with multiple breeding females. I used population monitoring data for wolves in Idaho and Yellowstone National Park, Wyoming, United States as well as genetic pedigree data for a subset of wolf groups that contained multiple breeding females in Idaho. High wolf density and large group size were both associated with a significant increase in the frequency of multiple breeding females in a group. The probability a pup survived their first year was related positively to the number of breeding females in a group. Multiple breeding can also take the form of polyandry, and “sneaker” males were responsible for paternity in nearly 13% of pups born. Breeding strategies in this social carnivore may be more variable than previously assumed, but their occurrence can be predicted by group size and density. Wolf population projection models and studies regarding reproduction and cooperative breeding in wolves would benefit by incorporating the potential for multiple breeding individuals. Genetic models in particular will be more reliable if they incorporate the potential effect of sneaker males on genetic diversity in a population.
Carnivores that exhibit fission–fusion social organization can adapt group sizes to prevailing social and ecological conditions. This study focuses on social organization of African lions (Panthera leo) in the Okavango Delta, a seasonally flooded wetland. We used generalized estimating equations and generalized linear mixed models to estimate the effects of flooding, as well as prey availability and intraspecific competition on group sizes of lions. During years of high flood, total lion pride sizes as well as reproductive rates declined. Prides showed extensive overlap in annual home ranges, likely as a result of habitat saturation at high densities, and pride sizes were not limited by prey availability. At the subgroup level, the number of attending cubs was the most consistent predictor of subgroup size of adult females. For subgroups without cubs, higher numbers of neighbors in adjacent, competing prides resulted in larger subgroups in focal prides, likely to maintain numerical advantage in inter-pride encounters. Larger subgroups were also formed in response to greater availability of large prey, as successfully hunting large prey requires a greater degree of cooperation. In the southwestern Okavango Delta, competition for space resulting from changing flooding regimes is a greater limiting factor for total pride sizes than food availability.
Flávia P. Tirelli, Tatiane C. Trigo, Cristine S. Trinca, Ana Paula N. A lbano, Fábio D. Mazim, Diego Queirolo, Caroline da C. Espinosa, José Bonifácio Soares, Javier A. Pereira, Peter G. Crawshaw, David W. Macdonald, Mauro Lucherini, Eduardo Eizirik
Geoffroy's cat (Leopardus geoffroyi) is a small Neotropical felid whose social behavior remains poorly understood. We used simultaneous radiotelemetry (4 males and 3 females) and camera trapping to examine the spatial structure and dynamics of a population of this species in the Brazilian pampas (part of the Uruguayan Savannah ecoregion), including assessment of interindividual genetic relatedness. Home ranges (HRs) and core areas of males were larger than those of females. Males were significantly heavier than females, and linear regression analyses indicated that body mass of males significantly influenced HR size, whereas the relationship was not significant for females. When we performed a joint analysis comparing our data to those reported previously for other study sites, we observed the same patterns. We detected extensive HR and core area overlap among most of our monitored individuals, with no clear sex-based pattern. Moreover, our molecular data indicated that most of the sampled individuals were unrelated, and that the levels of HR and core area overlap were not significantly influenced by genetic relatedness. These results suggest that some interindividual tolerance and relaxation in territoriality may occur in Geoffroy's cat. We detected only minor changes in HR and core area size and overlap between seasons, indicating that the spatial structure we observed was temporally stable. On a broader perspective, our cross-site comparisons illustrate the usefulness of performing multiple ecological studies employing comparable methods at different locations to better understand the ecology of wild felid populations.
Worldwide, private lands have attracted increased attention from conservationists, not only because most of the globe is privately owned, but also because private lands can be an asset to the protected area conservation strategy. In Brazil, the riverine Areas of Permanent Protection (APPs) are a key instrument of the Forest Code to protect biodiversity on private lands, acting as wildlife corridors. We assessed this putative role of APPs by evaluating how ocelot (Leopardus pardalis) occurrence is influenced by covariates in 3 cerrado landscapes dominated by sugarcane and managed forests of eucalyptus and pine trees. We collected detection–nondetection data by camera trapping during 2 dry seasons (2013 and 2014) at 208 stations (6,606 camera-days). We estimated ocelot detection and mean relative abundance using a single-species, single-season occupancy model that accounts for heterogeneous detection probability induced by variation in abundance. Modeling results showed that percentage of native forest was the most important covariate to explain mean relative abundance of ocelots. This parameter was also affected positively by APPs, with ocelots being more abundant inside than outside APPs and, unexpectedly, by sugarcane. Given our study design, however, the positive effect of this crop likely reflects the contact zone between sugarcane and native forest. Our findings show that landscape composition affects ocelot abundance and highlight the importance of APPs and Legal Reserves in agricultural landscapes. We conclude that, in such landscapes, compliance to the Forest Code by private land owners is key to supporting ocelot occurrence.
Alexander Gavashelishvili, Yuriy A. Yarovenko, Elmar A. Babayev, Giorgi Mikeladze, Zurab Gurielidze, Davit Dekanoidze, Niko Kerdikoshvili, Levan Ninua, Nika Paposhvili
Our research attempts 1) to link the distribution and abundance of eastern tur (Capra cylindricornis) to environmental variables varying in space and time, and 2) to identify environmental constraints that may have caused the geographic segregation of eastern tur from western tur (Capra caucasica). Our results suggest that 1) eastern tur are heat-sensitive but prefer snow-free, grass-dominated areas near escape cliffs, and in terrain that is difficult for humans and livestock to reach; and 2) present-day genetic and phenotypic differences between the Capra species are largely related to discontinuity of and impeded migration between Capra populations during glacial periods, and insufficient time in the postglacial period for now-adjoining Capra populations to overcome behavioral mechanisms impeding hybridization in the wild so as to erase these differences.
The black-eared mouse Peromyscus melanotis is distributed in conifer forests and highland prairies throughout the Trans-Mexican Volcanic Belt, Eastern Sierra Madre and Western Sierra Madre in Mexico, and isolated mountain ranges in Arizona, United States. We examined geographic variation in cranial measurements throughout the distribution of the species in Mexico. Because populations of these major ranges are isolated, we expected discontinuities in variation consistent with geographic gaps. Instead, we found no differences between the Sierras and significant differences between them and the Trans-Mexican Volcanic Belt. Moreover, a north-to-south trend of size increase was detected. By relating size to 6 environmental variables, we evaluated 4 hypotheses previously proposed to explain the observed pattern of variation: 1) seasonality, 2) body heat conservation or Bergmann's rule, 3) primary productivity, and 4) body heat dispersion. Significant positive correlations with elevation, productivity, and humidity, and negative correlations with annual mean temperature, temperature seasonality, and latitude led us to conclude that the observed pattern of variation in size is not related to body heat conservation or loss, but driven by primary productivity, a positive correlate of resource availability.
Andean and Pampas cats are 2 Neotropical small felids of the genus Leopardus. Until now, most of the scarce morphometric data published for these felids, especially the rare Andean cat (L. jacobita), were obtained from museum skins and skulls of undetermined sex. Here, we present morphological data from Pampas cats (L. colocolo) and the largest sample of live Andean cats (5 Andean cats and 6 Pampas cats) captured in the Argentine High Andes. We provide a craniometric analysis of all available adult skulls of Andean cats, including the first known female specimens of Andean and Pampas cats (n = 42). We nearly double the number of published external measurements for live Andean cats, and provide measurements and photos of all available skulls of adult Andean cats, including 2 new skulls with known sex. The data show that Andean cats are larger than Pampas cats and morphometric differences may be related to sexual dimorphism in both species. Principal component analysis of skull measurements showed almost complete separation of Andean and Pampas cats.
The pigmentation patterns of Indo-Pacific humpback dolphins have not been well studied throughout most of the species' range. In the present study, both the subjective scoring method and a newly developed quantified scoring method were employed to evaluate the spotting intensity of 137 humpback dolphin individuals from the Xiamen and Beibu Gulf putative populations, including the Dafengjiang-Nanliujiang River Estuary (DRE) and Shatian-Caotan (SC) communities. Both scoring methods indicated that spotting intensity on the dorsal fin was lower than that on the body of humpback dolphins in all 3 groups. The SC and DRE humpback dolphins had significantly greater dorsal fin, body spotting intensity, and greater differences between spotting on the dorsal fin and body than Xiamen dolphins, while no differences were found between SC and DRE. The pigmentation variation is related to age class, young dolphins have more spotting density than adults, and young and adults showed similar geographical variation as above. The present paper, in combination with previous research, clarifies the general pattern of pigmentation for Chinese humpback dolphins. Eastern Taiwan Strait and Pearl River Estuary populations represent 2 extreme patterns of pigmentation, while the Xiamen population, SC community, and DRE community seem to be intermediate. The results suggest that these groups should be viewed as demographically distinct forms.
Population genetic patterns can be affected by a number of factors, including life history characteristics and landscape features. Identifying general patterns of connectivity and key factors affecting these patterns is often central to effective ecological monitoring and management, particularly in areas with increasing urbanization. Examining patterns of connectivity and diversity of widespread and still abundant vertebrates, such as many cricetid rodents, can serve as a general indicator of habitat quality and connectivity. We investigated patterns of genetic diversity, differentiation, and population structure in 2 species of deer mice (Peromyscus californicus and P. fraterculus) occupying patches of native habitat separated by roadways in San Diego County, California. The 2 species are closely related and frequently co-occur at the same site. We collected samples from 5 widely distributed sites throughout the county and analyzed them using 10–12 microsatellites. We found similar levels of genetic diversity in both species, with allelic richness ranging from 4.47 to 8.81 and observed heterozygosity values from 0.60 to 0.79. In general, we found that P. californicus exhibits a pattern of isolation by distance at a finer spatial scale than does P. fraterculus. Populations of both species that were separated by major roads were not strongly genetically differentiated, with one exception: at 1 site, P. fraterculus exhibited signs of minor differentiation across a roadway. However, subsequent landscape modeling at this site was unsuccessful in detecting a correlation between specific landscape features and genetic differentiation. In general, our study shows that small rodent populations may be robust with respect to impacts of recent anthropogenic fragmentation by roadways.
Habitat loss and fragmentation are likely to affect individual condition as they usually alter the quality of habitat. However, responses of individuals of different species to these processes may be subtle and difficult to detect, despite that such responses may reveal interesting and diverse strategies of persistence of species in fragmented landscapes. Here, we used model selection to 1) compare the body condition (Scaled Mass Index) of 2 Neotropical marsupials (Didelphis aurita and Philander frenatus) from 6 continuous forest sites and 25 forest fragments, and 2) determine whether local habitat structure and landscape and temporal factors affect body condition in forest fragments. Body condition of both species was lower in forest fragments compared to continuous forest sites, but only in the super-humid season for D. aurita and in the humid season for P. frenatus. When only forest fragments were compared, body condition of D. aurita was higher in the humid season, in sites with fewer Cecropia trees and water courses, lower percent forest cover, and surrounded by a mixed matrix (plantation and cattle ranching), or located in small rural properties. Body condition of P. frenatus was slightly higher in the super-humid season, in sites surrounded by a mixed matrix, with fewer Cecropia trees and water courses, more lianas, and greater percent forest cover. Our results revealed negative effects of habitat loss and fragmentation on both species, but also different responses of each species to local extrinsic environmental factors. We suggest that body condition should not be used as a direct indicator of animal fitness or habitat quality. Nonetheless, body condition may still reveal subtle and previously undetected responses of species to habitat disturbance and fragmentation.
We used Cormack–Jolly–Seber capture–recapture analyses to investigate differences in monthly survival of the southeastern beach mouse (Peromyscus polionotus niveiventris) between sexes, between juveniles and adults, and effects due to the presence of transients that can bias survival estimates. We accounted for transients (e.g., nonresidents) by distinguishing survival for the initial month after an individuals' 1st capture from monthly survival after the 1st recapture. Survival estimates for 1st captures and recaptures of females were 0.70 and 0.78, respectively. Survival estimates for 1st captures and recaptures of males were 0.74 and 0.80, respectively. Our results showed that a comparably small proportion of transients (females = 0.10; males = 0.08) can bias survival estimates.
Plant diets of 2 sympatric species of wood mice in Japan (Apodemus argenteus and A. speciosus) were determined by DNA meta-barcoding analyses of feces using the nucleotide sequences of the chloroplast trnL P6 loop intron region as a molecular marker. The 2 species showed a relatively large degree of niche overlap in plant dietary profiles, feeding mostly on acorn-producing Fagaceae species (assumed to be Quercus crispula). However, A. argenteus was less dependent on Fagaceae species than A. speciosus. Instead, A. argenteus had a wider niche breadth, feeding upon a wider range of plant families such as Betulaceae, Fabaceae, Oleaceae, Pinaceae, Rutaceae, Sapindaceae, Tiliaceae, and Ulmaceae, which were consumed only infrequently by A. speciosus. There was also evidence for species differences in diet across seasons. Oleaceae species (assumed to be Fraxinus mandshurica) were consumed by A. argenteus from June to August, and by A. speciosus from August to October. The results suggested that A. argenteus is a generalist feeder, and A. speciosus a specialist, and the 2 Apodemus species separate their dietary niches not only by the component plant species overall, but also by differences within seasons.
Molossops temminckii is the only species of the Molossidae capable of exploring background-cluttered space. We tested the hypothesis that M. temminckii uses the clutter rejection strategy in cluttered environments and determined whether the echolocation calls of this species show large-scale geographic variation. We recorded echolocation calls of 10 individuals of M. temminckii using 4 treatments with different degrees of clutter. We compared individuals recorded in Venezuela with individuals recorded in Brazil to verify geographic variation in calls. In the cluttered environments, M. temminckii emitted short downward frequency-modulated calls with short pulse intervals. In the uncluttered environments, M. temminckii emitted long upward frequency-modulated calls with longer intervals and shorter bandwidth. The decreased pulse duration and interval in cluttered environments support the hypothesis that M. temminckii uses the clutter rejection strategy. Additionally, we found that in Brazil, M. temminckii emits shorter calls with higher minimum frequency compared with bats recorded in Venezuela, indicating large-scale geographic variation, probably because of environmental factors.
Molossops temminckii é a única espécie de Molossidae com capacidade de explorar áreas com obstáculos de fundo. Nesse trabalho testamos a hipótese do uso da estratégia de rejeição de obstáculo em ambientes fechados, e determinamos se há variação geográfica de larga escala nos chamados de ecolocalização de M. temminckii. Gravamos 10 indivíduos, em 4 tratamentos, com diferentes graus de obstáculos. Comparamos os chamados de ecolocalização gravados na Venezuela e Brasil para verificar a variação geográfica. Em ambientes com obstáculos, M. temminckii emite chamados curtos, de frequência modulada descendente, com intervalos curtos entre os chamados. Nos ambientes abertos, emite chamados longos, de frequência modulada ascendente, com intervalos mais longos e menor largura de banda. A menor duração e o menor intervalo em ambientes fechados suportam a hipótese que M. temminckii utiliza a estratégia de rejeição de obstáculo. No Brasil, M. temminckii emite chamados mais curtos, com frequência mínima mais alta, em comparação com os morcegos gravados na Venezuela. Esse fato indica variação geográfica de larga escala e fatores ambientais provavelmente contribuem para essa variação.
Bat flight membranes are critical for locomotion, foraging, and physiological homeostasis. Wild bats frequently injure their flight membranes during interactions with the environment and conspecifics or from disease. Researchers biopsy bat wing membranes to mark individuals or collect tissue for taxonomic and molecular studies. Because there are differences in the embryological development of different wing membrane regions, we evaluated differences in flight membrane healing between 2 anatomical regions using 4-mm diameter circular biopsies in the chiropatagium and plagiopatagium of the Egyptian fruit bat (Rousettus aegyptiacus; Pteropodiformes) and the insectivorous big brown bat (Eptesicus fuscus; Vespertilioniformes). In R. aegyptiacus, plagiopatagium wounds took longer to heal to 50% of their initial area compared to chiropatagium wounds; however, this difference was not observed in E. fuscus. Plagiopatagium wounds also were more likely to enlarge in the days immediately following biopsy in R. aegyptiacus compared to E. fuscus. A sigmoid function accurately modeled wound areas and thus healing times in both species. Given the observed differences in wound-healing times between distinct regions of the bat wing membrane, our results indicate that researchers should choose a tissue biopsy location based on the species and question of interest.
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