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Nicholas J. DeCesare, Byron V. Weckworth, Kristine L. Pilgrim, Andrew B. D. Walker, Eric J. Bergman, Kassidy E. Colson, Rob Corrigan, Richard B. Harris, Mark Hebblewhite, Brett R. Jesmer, Jesse R. Newby, Jason R. Smith, Rob B. Tether, Timothy P. Thomas, Michael K. Schwartz
Subspecies designations within temperate species' ranges often reflect populations that were isolated by past continental glaciation, and glacial vicariance is believed to be a primary mechanism behind the diversification of several subspecies of North American cervids. We used genetics and the fossil record to study the phylogeography of three moose subspecies (Alces alces andersoni, A. a. gigas, and A. a. shirasi) in western North America. We sequenced the complete mitochondrial genome (16,341 base pairs; n = 60 moose) and genotyped 13 nuclear microsatellites (n = 253) to evaluate genetic variation among moose samples. We also reviewed the fossil record for detections of all North American cervids to comparatively assess the evidence for the existence of a southern refugial population of moose corresponding to A. a. shirasi during the last glacial maximum of the Pleistocene. Analysis of mtDNA molecular variance did not support distinct clades of moose corresponding to currently recognized subspecies, and mitogenomic haplotype phylogenies did not consistently distinguish individuals according to subspecies groupings. Analysis of population structure using microsatellite loci showed support for two to five clusters of moose, including the consistent distinction of a southern group of moose within the range of A. a. shirasi. We hypothesize that these microsatellite results reflect recent, not deep, divergence and may be confounded by a significant effect of geographic distance on gene flow across the region. Review of the fossil record showed no evidence of moose south of the Wisconsin ice age glaciers ≥ 15,000 years ago. We encourage the integration of our results with complementary analyses of phenotype data, such as morphometrics, originally used to delineate moose subspecies, for further evaluation of subspecies designations for North American moose.
Steller sea lions (Eumetopias jubatus) are composed of two genetically distinct metapopulations (an increasing “eastern” and a reduced and endangered “western” population, or stock for management purposes in U.S. waters) that are only recently mixing at new rookeries in northern Southeast Alaska, east of the current stock boundary. We used mark-recapture models and 18 years of resighting data of over 3,500 individuals marked at the new rookeries and at neighboring long-established rookeries in both populations to examine morphology, survival, and movement patterns of pups born at new rookeries based on whether they had mitochondrial DNA haplotypes from the western or eastern population (mtW or mtE); examine survival effects of dispersal to the Eastern Stock region for animals born in the Western Stock region; and estimate minimum proportions of animals with western genetic material in regions within Southeast Alaska. Pups born at new rookeries with mtW had similar mass, but reduced body condition and first-year survival (approximately –10%) compared to pups with mtE. mtE pups ranged more widely than mtW pups, including more to the sheltered waters of Southeast Alaska's Inside Passage. Fitness benefits for western-born females that dispersed to Southeast Alaska were observed as higher female survival (+0.127, +0.099, and +0.032 at ages 1, 2, and 3+) and higher survival of their female offspring to breeding age (+0.15) compared to females that remained west of the boundary. We estimated that a minimum of 38% and 13% of animals in the North Outer Coast–Glacier Bay and Lynn Canal–Frederick Sound regions in Southeast Alaska, respectively, carry genetic information unique to the western population. Despite fitness benefits to western females that dispersed east, asymmetric dispersal costs or other genetic or maternal effects may limit the growth of the western genetic lineage at the new rookeries, and these factors require further study.
Gray seals were historically distributed along the northeastern coast of the United States, but bounties and lack of protection reduced numbers and they were rarely observed for most of the 20th century. Once protections were enacted, the population started to rebound. Here, we describe the recolonization and recovery of gray seals in the United States, focusing on the re-establishment of pupping sites. We fit individual generalized linear models to various time series (1988–2019) to estimate rates of increase in observed pup counts at four of the more data-rich sites. Annual rate of increase at individual sites ranged from –0.2% (95% CI: –2.3–1.9%) to 26.3% (95% CI: 21.6–31.4%). The increase in sites and number of pups born in the United States is driven by population growth and immigration from Canadian colonies and is part of a larger recovery of the Northwest Atlantic population. Wildlife protection, a healthy source population, habitat availability, and species traits that allow for dispersal and high productivity were all important factors in this recovery.
Suisun Marsh (Solano County, California) is the largest contiguous marsh remaining on the West Coast of the United States, and makes up approximately 10% of the wetlands remaining in the San Francisco Estuary. Suisun Marsh has been safeguarded from development through the operation of over 100 privately owned waterfowl hunting clubs, which manage for diked waterfowl habitat. However, this management—and the subsequent loss of tidal influence—has been considered harmful for some species, including the endangered salt marsh harvest mouse (SMHM; Reithrodontomys raviventris). To determine the value of tidal wetlands relative to those managed for waterfowl, we performed periodic surveys for rodents in managed and tidal wetlands over 5 years, and used capture-mark-recapture analyses to estimate demographic parameters and abundance for the three most common rodents—the northern SMHM (R. r. halicoetes), the western harvest mouse (a sympatric native species; R. megalotis, WHM), and the house mouse (a sympatric invasive species; Mus musculus). Wetland type had no effect on detection, temporary emigration, or survival for any of these species. However, fecundity and population growth for all three species were affected by an interaction of season and wetland type, although none of these parameters was consistently superior in either habitat type. Estimated abundance of SMHM and Mus was similar in both wetland types, whereas WHM were more abundant in managed wetlands. Salt marsh harvest mice also showed no affinity for any microhabitat characteristics associated with tidal wetlands. Managed wetlands in Suisun Marsh support SMHM and Mus equally, and abundances of WHM were greater than in tidal wetlands, suggesting managed wetlands may be superior in terms of supporting native rodents. As climate change and sea level rise are predicted to threaten coastal marshes, these results suggest the recovery strategy for SMHM could incorporate managed wetlands.
The nine-banded armadillo (Dasypus novemcinctus) is unique among mammals because females produce litters of genetically identical quadruplets via monozygotic polyembryony. This unusual form of reproduction could have profound impacts on the spatial genetic structure of populations of armadillos, but at present it is unclear whether littermates remain together as adults, or if sex-biased dispersal occurs. The goal of our study was to determine whether fine-scale spatial genetic structure (FSGS) within a population of armadillos diminishes with age (i.e., from juvenile to adult due to the dispersal of littermates away from one another), and if the degree of FSGS for a given age class differs between the sexes. We obtained genotype data at seven microsatellite DNA loci for 421 individuals in a wild population of armadillos inhabiting the Yazoo National Wildlife Refuge in western Mississippi. Correlogram analyses based on measures of spatial genetic autocorrelation showed weak but significant FSGS that was driven by positive spatial genetic autocorrelation among both male and female juveniles and adult males, but not adult females. Positive spatial genetic autocorrelation among adult males could be due to either female-biased dispersal or high variance in male reproductive success. Further work is required to discriminate between these two possibilities.
The giant armadillo (Priodontes maximus) is the largest living armadillo. This naturally rare and poorly known species is endemic to South America and classified as “Vulnerable” by the IUCN. Here we explored aspects of the spatial ecology of P. maximus in Midwestern Brazil to gain insights on its ecology and biology to support conservation efforts. In 8 years, we identified 50 individuals of P. maximus and monitored 23 of them using telemetry methods. To characterize site fidelity and home range, we fitted individual continuous-time movement models and estimated Autocorrelated Kernel Density Estimates. We built a Structural Equation Model to evaluate how home-range area and daily displacement are related to each other, to sampling effort, and to individual characteristics. We estimated home-range overlap between pairs of different sexes using a bias-corrected Bhattacharyya coefficient. Finally, we formulated a canonical density estimation formula to characterize minimum population density. We gathered a total of 12,168 locations of P. maximus. The best-fitted movement models indicated site fidelity for all individuals and a median adult home-range area of 2,518 ha. Median adult daily displacement was 1,651 m. Home-range area scales positively with daily displacement and daily displacement scales positively with body mass. Median home-range overlap between pairs was low (4%) and adult females presented exclusive home ranges among themselves. Median minimum density was 7.65 individuals per 100 km2 (CI = 5.68–10.19 ind/100 km2). Our results are congruent with characterizing P. maximus as a generally asocial species, most likely promiscuous/polygynous, that establishes large, long-term home ranges, which grants the population a naturally low density. Spatial patterns and biological characteristics obtained in this study can be used to guide future conservation strategies for P. maximus in the Pantanal wetlands and elsewhere.
Felipe Rocha, Francisco Miroslav Ulloa-Stanojlovic, Vanessa Cristina Victor Rabaquim, Paulo Fadil, Júlio César Pompei, Paulo Eduardo Brandão, Ricardo Augusto Dias
The vampire bat (Desmodus rotundus) plays a crucial role in the maintenance and transmission of the rabies virus to humans and livestock, impacting public health and economic production. Its importance lies not only in its capacity to transmit the virus but also in its ability to adapt to anthropic changes, as expressed in its wide geographic distribution in Latin America. Deforestation, livestock intensification, and other human activities have reduced the abundance of its wild prey but have also provided new and abundant shelter and foraging resources for the vampire bats. We used radiotelemetry to evaluate relations between topography, feeding site choice, and foraging behavior in southeastern Brazil, where three occupied D. rotundus roosts, out of 11 possible, were systematically monitored throughout a 1-year period once every 2 months. Sixty-two vampire bats were captured; biometric data were collected and 44 radiotransmitters were installed in adult individuals, producing telemetry data that were recorded in VHF receptors installed in the farms. Elevation of the roosts was related to the farms attacked by the vampire bats. Understanding the use of the environment and resources by vampire bats is critical to improving rabies control aiming at the reduction of disease impacts. From the perspective of the official veterinary service, telemetry would be ineffective as a rabies surveillance system due to the costs and limitations of the available technology. However, livestock rabies control measures would be greatly improved if ecological characteristics of the vampire bat were considered.
The northern long-eared bat (Myotis septentrionalis) is currently listed as threatened under the U.S. Endangered Species Act largely due to population declines resulting from the spread of white-nose syndrome in North America. White-nose syndrome was confirmed in Iowa in 2015, emphasizing a need to closely monitor populations of M. septentrionalis statewide. We applied presence-only models to predict landscape-scale resource selection by M. septentrionalis using roost tree observations and mist net captures from various research and environmental assessment projects in Iowa (2003–2015). We used a simultaneous autoregressive (SAR) model to account for residual spatial autocorrelation in our compiled data set and estimate the proportional probability of use of summer habitats for M. septentrionalis. We estimated SAR models using four environmental predictor variables measured at two landscape scales (0.5- and 2.4-km) representative of M. septentrionalis home range sizes in North America. The SAR models resulted in high predictive fit with withheld test observations and an independent data set of acoustic detections of M. septentrionalis from recent surveys (2016–2018), indicating a significant positive relationship existed between habitat quality (as an index of selection) and distribution of M. septentrionalis at landscape scales. At both spatial scales, M. septentrionalis showed positive selection of closed canopy interior forest, bottomland hardwood forest, and total perennial stream length, whereas at the 0.5-km scale, M. septentrionalis also showed a positive association with open canopy forest. Our models indicated that up to 7.0% and 8.5% of the state was comprised of potentially suitable forested summer habitats for M. septentrionalis for 0.5- and 2.4-km scales, respectively. Our models also indicated the distribution of highly selected habitats at landscape scales in Iowa and accurately predicted independent observations of M. septentrionalis in areas of the state where no capture efforts have occurred. This study provides methods to predict landscape-scale resource selection and distribution for bats where multiple fine-scale data sources exist across broad geographic regions.
Knowledge of the spatiotemporal variability of abundance and vital rates is essential to the conservation of wildlife populations. In Pacific Northwest forests, previous small mammal research has focused on estimating abundance; few studies have focused on vital rates. We used robust design temporal symmetry models and live-trapping data collected 2011–2016 at nine sites to estimate apparent annual survival, population growth rate, and recruitment of Humboldt's flying squirrels (Glaucomys oregonensis) and Townsend's chipmunks (Neotamias townsendii) in a late-successional forest of the Cascade Mountains of Oregon, United States. We also estimated the proportional contribution of apparent annual survival and recruitment to population growth rate. Covariates previously associated with abundance were also associated with vital rates for Townsend's chipmunks, but less so for Humboldt's flying squirrels. Apparent annual survival was nearly constant (range = 0.47 to 0.51) among years and sites for Humboldt's flying squirrels but was consistently lower and more variable among years for Townsend's chipmunks (range = 0.13 to 0.31). Recruitment was variable among years for both species. Apparent annual survival generally contributed more than recruitment to the population growth rate of Humboldt's flying squirrels. For Townsend's chipmunks, recruitment consistently contributed more than apparent annual survival to population growth rate. These findings suggest that life history strategies differed for these co-occurring species. This study demonstrates substantial temporal variation in vital rates and some differences in abundance and vital rate habitat associations, suggesting that habitat suitability inferences based on short time series or variation in abundance could be misleading.
The North American badger (Taxidea taxus) is a nonhibernating carnivore that occurs in areas with highly seasonal climates, such as in Canada where the animal reaches its northern limits. There, winter climate is harsh and conventional habitat is limited and patchy, possibly leading to additional energetic constraints. Using radiotelemetry and remote cameras, we documented winter activities of 16 badgers (12 females, 4 males) between 2007 and 2011 in British Columbia, at the northwestern periphery of the species' range. In comparison to their summer ecology, the animals reduced home range sizes by up to 98% and showed fidelity to particular burrows. Burrow fidelity was variable (mean 27 days; range 0–108) and coincided with reduction in body temperatures, suggesting the onset of torpor. Despite lengthy use of the same burrow, badgers emerged frequently and conducted excursions that appeared to represent foraging behavior. Burrow emergence was not related to ambient temperature or snow depth; rather, it was best explained by the amount of days elapsed since the start of winter. Despite these trends, winter activity also was variable among individual badgers. It may be that limited fat reserves and higher energetic costs in northwestern ranges require winter foraging activities.
Eurasian otters (Lutra lutra) are known to make extensive use of reservoirs in the Iberian Peninsula, where they forage preferentially on small-size fish (10–20 cm). We hypothesized that the usual consumption of small-size fish by otters in reservoirs is not due to prey size preference, but rather to a higher level of difficulty in capturing larger prey. We studied otter diet in a reservoir that experienced an abrupt drop in stored water caused by an unusually severe drought. We compared relative prey size, hunting success, and diving times between the year of the drought (2017) and two standard rainfall years (2015 and 2016). Otters ate a similar proportion of small and large fish during the drought instead of predominantly eating small fish. Mean diving time during the drought was similar to that of the standard climatic years, indicating a similar physiological cost of capture between small and large fish. Otters had higher hunting success in the drought year (89%) than in the standard years (63%) regardless of prey size. This suggests a higher level of catchability of both fish size classes during the drought as the water level was lower. Results suggest that the usual consumption of small-sized fish by otters in reservoirs could not be related to preference or relative abundance but rather to the difficulty of capturing large-size fish when water levels are high.
The Flint Hills represent the largest tract of tallgrass prairie in North America and is located near the western edge of the native range of the Virginia opossum (Didelphis virginiana). This region is undergoing rapid landscape changes (e.g., urbanization, agriculture, woody encroachment) that are negatively affecting mammal communities. Although previous research has revealed northward distributional expansions of Virginia opossums facilitated by urban development, no studies have assessed how landscape change affects distribution patterns along the western edge of their geographic range. During 2016–2018, we monitored site (n = 74) occupancy along urban–rural transects in the Flint Hills to assess the influence of landscape change (i.e., urban, grassland, agriculture, woody encroachment) and water availability on the distribution of Virginia opossums. Sites surrounded by urban land cover had greater initial occupancy probabilities and lower extinction rates. Sites closer to permanent water sources experienced greater colonization rates and lower extinction rates. In addition, site extinction rates were lower in areas surrounded by woody encroachment. Our results concur with other studies suggesting that growing urban areas may expand opossum distributions along the edges of their geographic range. Our study also suggests that woody encroachment into tallgrass prairies may provide an alternative pathway for future distributional expansions. Future research must consider the potential for landscape change, along with dynamic water availability, in models predicting the distribution of Virginia opossums.
Foraging animals choose habitats based on characteristics that often cannot be satisfied simultaneously, such as easy mobility, abundant or high-quality foods, and safety from predators. Invasive plants may alter habitat structure and provide novel foods; thus, measuring how animals forage in invaded landscapes offers insights into these new ecological relationships. We examined the movements of Great Basin pocket mice (Perognathus parvus) in sage-steppe habitats invaded by cheatgreass (Bromus tectorum) in southcentral British Columbia, Canada. The pathway tortuosity (fractal D) of pocket mice increased with vegetative cover and population density and decreased with open habitat, but these variables explained little of the variation in tortuosity. The fractal dimension of movement pathways of pocket mice was consistent over spatial scales ranging from 0.5 m to two-thirds of the home range size, unlike in other species where fractal dimensions are not consistent over multiple spatial scales. Collectively, our results indicate that foraging movements of pocket mice were not affected by the low densities of cheatgrass in this system.
Romeo A. Saldaña-Vázquez, Jorge Ortega, José Antonio Guerrero, M. Isabel Aiza-Reynoso, M. Cristina MacSwiney G, Pedro A. Aguilar-Rodríguez, Jorge Ayala-Berdon, Veronica Zamora-Gutierrez
Phenology in animals is strongly influenced by seasonality that promotes changes in abundance of food resources and temperature. These changes may impose energetic constraints to organisms in certain seasons during the year, especially on those animals facing high energetic demands, such as nectarivorous bats. Seasonality in temperate forests could, therefore, promote migration of female nectarivorous bat to find warmer sites, thus enhancing breeding success. To test this hypothesis, we compared the proportion of females and the proportion of pregnant females of the nectarivorous bat Anoura geoffroyi, between months, in six different populations across temperate forests of Mexico. Bats were captured over a complete season cycle either with sweep or mist nets at the entrance or near their roosting caves, and their age, sex, and reproductive condition were recorded. We found that over 50% of bats present in the cave roosts across different populations in temperate forests of the Trans-Mexican Neovolcanic Belt of Mexico during the warmer and wetter months (April–September) were females, both pregnant and nonpregnant. In contrast, fewer than 30% of bats present in the roosting caves sampled in the colder and drier months (October–March) were females. In addition, we found that the temperature that favors the proportion of females at the studied sites was greater than 8°C. We concluded that seasonality affects sex ratio and phenology of A. geoffroyi in Mexican temperate forests. Our findings suggest females' migrations to lowland warmer sites to improve prenatal development.
Necromys is a genus of sigmodontine rodent that inhabits grasslands and scrublands in South America. Eight extant species are recognized in the genus; one of these is Necromys lactens, which inhabits high-elevation grasslands in the Yungas from south-central Bolivia to northwestern Argentina. Morphological variation in N. lactens has been recognized by the description of three nominal forms. Geographically structured genetic diversity also has been observed, but a thorough revision of these nominal forms within an integrative framework has yet to be performed. We conducted a phylogeographic assessment based on an 801 base-pair fragment of the cytochrome-b gene that guided morphometric analyses (univariate and multivariate comparisons) of patterns of geographic variation in the species, and the distinction of its nominal forms. Haplotypes of N. lactens form a well-supported and geographically structured clade. Within it, there are two main clades; haplotypes from the northern range form a well-supported clade, sister and allopatric to a weakly supported southern clade, which includes variants collected at or near the type localities of three nominal forms. In turn, both main clades are composed by two allopatric subclades. Morphometric analyses indicated no differences in shape of the skull among the three nominal forms or between the recovered clades and subclades. Taking together all the available evidence, we consider N. lactens to be a monotypic species.
The reproductive season of white-tailed deer (Odocoileus virginianus) has been hypothesized to be aseasonal south of about 14°–18°N latitude, where annual variation in day length is low. We tested this idea by using camera-trap data (1,336 photographed individuals identified by age and sex) collected during 2011–2017 in the dry tropical forest of Santa Rosa National Park, northwest Costa Rica, where wet and dry seasons are well-defined. We identified variation in monthly occurrence of spotted deer fawns, as well as the status of antler growth of male deer, specifically related to the very seasonal environment of the region. Year-round reproduction likely occurs, but the rainfall pattern in the area greatly influences the relative frequency of reproductive indicators, with most births occurring during the dry season, and a second peak occurring toward the latter part of the wet season. We speculate that food resources are the major influence on reproductive patterns, and that variation in types and timing of food resource availability likely account for the variation in reproductive patterns.
Behavioral plasticity, or the mechanism by which an organism can adjust its behavior in response to exogenous change, has been highlighted as a potential buffer against extinction risk. Giraffes (Giraffa spp.) are gregarious, long-lived, highly mobile megaherbivores with a large brain size, characteristics that have been associated with high levels of behavioral plasticity. However, while there has been a recent focus on genotypic variability and morphological differences among giraffe populations, there has been relatively little discussion centered on behavioral flexibility within giraffe populations. In large wild herbivores, one measure of behavioral plasticity is the ability to adjust herd size in line with local environmental conditions. Here, we examine whether a genetically isolated population of Angolan giraffes (G. g. angolensis) in a heterogeneous environment adjust their herd sizes in line with spatiotemporal variation in habitat. Our results suggest that ecological factors play a role in driving herd size, but that social factors also shape and stabilize herd-size dynamics. Specifically, we found that 1) mixed-sex herds were larger than single-sex herds, suggesting that sexual composition of herds played a role in driving herd size; 2) the presence of young did not influence herd size, suggesting that giraffes did not make use of the dilution effect to safeguard their young from predation; and 3) there was a strong relationship between herd size and spatial, but not seasonal, variation in food biomass availability, suggesting stability in herd sizes over time, but temporary variation in line with resource availability. These findings indicate that giraffes adjust herd size in line with local exogenous factors, signaling high behavioral plasticity, but also suggest that this mechanism operates within the constraints of the social determinants of giraffe herd size.
Musth is an annual, asynchronous, rut-like phenomenon observed in male elephants. We examined whether musth is a roving strategy, and whether musth provides a temporary advantage to young males through increased access to female groups. We collected long-term data on the musth status, associations, and locations of male elephants in the Kabini population in southern India. We sighted older males more frequently in musth than younger males. We found a greater turnover of musth than non-musth males in the study area, suggesting that musth is a roving strategy, enabling males to travel widely and away from their non-musth range. Contrary to our expectation, young (15–30 years old) males spent a smaller proportion of their musth time than their non-musth time associating with females, and associated with similarly sized female groups irrespective of musth status. Old (> 30 years old) males spent only a slightly higher proportion of their musth time than non-musth time with female groups, but associated with larger female groups during musth. Although old males in musth associated with young non-musth males more often in the presence, than in the absence, of females, young males in musth were never sighted with old non-musth males in the presence of females. Therefore, the payoff from musth, as a strategy to gain access to females, was age-specific; musth in old males allowed for increased association with females, while musth in young males restricted their access to females. There was no spatial avoidance between musth and non-musth adult males at scales larger than immediate associations. Our results suggest that musth seems to be primarily a roving strategy for old males to find and associate with females and not a strategy for young males to gain a temporary advantage over old males, within the broad age-classes that we examined.
Central-place foragers can be constrained by the distance between habitats. When an organism relies on a central place for thermal refuge, the distance to food resources can potentially constrain foraging behavior. We investigated the effect of distance between thermal refuges and forage patches of the cold-intolerant marine mammal, the Florida manatee (Trichechus manatus latirostris), on foraging duration. We tested the alternative hypotheses of time minimization and energy maximization as a response to distance between habitats. We also determined if manatees mitigate foraging constraints with increased visits to closer thermal refuges. We used hidden Markov models to assign discrete behaviors from movement parameters as a function of water temperature and assessed the influence of distance on foraging duration in water temperatures above (> 20°C) and below (≤ 20°C) the lower critical limit of the thermoneutral zone of manatees. We found that with increased distance, manatees decreased foraging duration in cold water temperature and increased foraging duration in warmer temperatures. We also found that manatees returned to closer thermal refuges more often. Our results suggest that the spatial relationship of thermal and forage habitats can impact behavioral decisions regarding foraging. Addressing foraging behavior questions while considering thermoregulatory behavior implicates the importance of understanding changing environments on animal behavior, particularly in the face of current global change.
Disturbances such as fire reduce the structural complexity of terrestrial habitats, increasing the risk of predation for small prey species. The postfire effect of predation has especially deleterious effects in Australian habitats owing to the presence of invasive mammalian predators, the red fox (Vulpes vulpes) and feral cat (Felis catus), that rapidly exploit burned habitats. Here, we investigated whether the provision of artificial shelter could alleviate the risk of predation perceived by two species of small marsupial, the dunnarts Sminthopsis hirtipes and S. youngsoni, in open postfire habitat in the sandridge system of the Simpson Desert, central Australia. We installed artificial shelters constructed from wire mesh that allowed passage of the dunnarts but not of their predators at one site, and measured and compared the perceived risk of predation by the dunnarts there with those on a control site using optimal patch-use theory (giving-up densities, GUDs). GUDs were lower near artificial shelters than away from them, and near dune crests where dunnarts typically forage, suggesting that the shelters acted as corridors for dunnarts to move up to the crests from burrows in the swales. Foraging was lower near the crest in the control plot. Two-day foraging bouts were observed in dunnart activity, with recruitment to GUD stations occurring a day earlier in the augmented shelter plot. Despite these results, the effects of the shelters were localized and not evident at the landscape scale, with GUDs reduced also in proximity to sparse natural cover in the form of regenerating spinifex grass hummocks. Mapping dunnart habitat use using the landscape of fear (LOF) framework confirmed that animals perceived safety near shelter and risk away from it. We concluded that the LOF framework can usefully assess real-time behavioral responses of animals to management interventions in situations where demographic responses take longer to occur.
Bartonella is a genus of gram-negative bacteria that includes a variety of human and veterinary pathogens. These pathogens are transmitted from reservoirs to secondary hosts through the bite of arthropod vectors including lice and fleas. Once in the secondary host, the bacteria cause a variety of pathologies including cat-scratch disease, endocarditis, and myocarditis. Reservoirs of these bacteria are numerous and include several species of large mammals, mesocarnivores, and small mammals. Research on reservoirs of these bacteria has focused on western North America, Europe, and Asia, with little focus on the eastern and central United States. We assessed the prevalence of zoonotic Bartonella species among prairie-dwelling rodent species in the midwestern United States. Tissue samples (n = 700) were collected between 2015 and 2017 from five rodent species and screened for the presence of Bartonella DNA via PCR and sequencing of two loci using Bartonella-specific primers. Bartonella were prevalent among all five species, with 13-lined ground squirrels (Ictidomys tridecemlineatus) serving as a likely reservoir of the pathogen B. washoensis, and other rodents serving as reservoirs of the pathogens B. grahamii and B. vinsonii subsp. arupensis. These results demonstrate the value of studies of disease ecology in grassland systems, particularly in the context of habitat restoration and human–vector interactions.
Molecular forensics is an important component of wildlife research and management. Using DNA from noninvasive samples collected at predation sites, we can identify predator species and obtain individual genotypes, improving our understanding of predator–prey dynamics and impacts of predators on livestock and endangered species. To improve sample collection strategies, we tested two sample collection methods and estimated degradation rates of predator DNA on the carcasses of multiple prey species. We fed carcasses of calves (Bos taurus) and lambs (Ovis aires) to three captive predator species: wolves (Canis lupus), coyotes (C. latrans), and mountain lions (Puma concolor). We swabbed the carcass in the field, as well as removed a piece of hide from the carcasses and then swabbed it in the laboratory. We swabbed all tissue samples through time and attempted to identify the predator involved in the depredation using salivary DNA. We found the most successful approach for yielding viable salivary DNA was removing hide from the prey and swabbing it in the laboratory. As expected, genotyping error increased through time and our ability to obtain complete genotypes decreased over time, the latter falling below 50% after 24 h. We provide guidelines for sampling salivary DNA from tissues of depredated carcasses for maximum probability of detection.
Crucial to the success of studies based on capture-mark-recapture (CMR) designs is the retention (permanency) and recognition (readability) of marks to identify individuals. Several marking methods for small mammals (< 60 g) are available, but their efficacy and use is not well known. We implemented a targeted survey of experts to gather their experiences and opinions regarding marking small mammals. Respondents (n = 114) stated their beliefs, perceptions, and current and future use, of marking methods, as well as factors influencing their choices, based on Likert and rank order scale questions. We compared responses based on where researchers' studies occurred, their level of experience, and their subfield of mammalogy. Most respondents (73%) had > 5 years experience marking small mammals, with 60% each marking > 1,000 individuals. Respondents believed that ear-tagging was most preferable in terms of efficiency, impact to affected animals (survival, pain), and personal ethics, whereas passive integrated transponder (PIT)-tagging was the most preferable with regard to retention and recognition, and toe-clipping with respect to cost. Most respondents plan to use ear-tagging (78%) or PIT-tagging (70%) in the future. PIT- and genetic-tagging are expected to increase, and toe-clipping to decline, in the future. The factors influencing which marking method respondents used were ranked—in order of decreasing preference—as impact, retention, recognition, cost, efficiency, and ethics. There were few differences in the mean response or consensus among respondents, regardless of their experience, location, or subfield. Most respondents (66%) agreed that additional studies on the performance and impact of various marking methods are needed to assess their costs and benefits for CMR-based studies. Ultimately, choice of marking method will depend on the species, research question, available resources, and local legislation and permitting. Our study, however, illustrates that collective insights by experienced mammalogists may aid individual researchers in deciding on study designs and protocols, particularly early career scientists.
Conservation efforts rely on robust taxonomic assessments that should be based on critical assessment of interspecific boundaries, infraspecific variation, and potentially distinctive peripheral populations. The meadow vole (Microtus pennsylvanicus) is widely distributed across North America, including 28 morphologically defined subspecies and numerous isolated populations. Because some subspecies are of high conservation concern, we examined geographic variation across the range of the species to test existing infraspecific taxonomy in terms of local and regional diversification. We sequenced mitochondrial DNA (mtDNA) from 20 subspecies of M. pennsylvanicus and contextualized infraspecific variation through comparison of pairwise genetic distances derived from an extended data set of 63 species of Microtus. We found strong support for at least three divergent clades within M. pennsylvanicus, with observed intraspecific clade divergence exceeding that between several pairwise comparisons of sister species within Microtus. Six nuclear genes were then sequenced to test the validity of mtDNA structure and to further evaluate the possibility of cryptic, species-level diversity using Bayes factor species delimitation (BFD) analyses. BFD consistently and decisively supported multiple species based on the multilocus approach. We propose that taxonomic revision of the meadow vole is required, with the eastern clade now identified as M. pennsylvanicus (Ord 1815), the western clade as M. drummondii (Audubon and Bachman 1853), and the coastal Florida clade as M. dukecampbelli (Woods, Post, and Kilpatrick 1982). We suggest that such an arrangement would more closely reflect evolutionary history and provide critical context for further examination of distinctive southern peripheral populations that harbor novel evolutionary legacies and adaptive potential.
The consumption of fruits and floral resources, as core or complementary food items, occurs in 75% of phyllostomid species. If phylogenetically related bat species have similar plant species in their diets, then it is expected that vegetal resources composition influences the phylogenetic structure of phyllostomid assemblages. We ask here if the phylogenetic structure of phyllostomid assemblages is associated with vegetation structure and resources. Our results showed that proportions of plant sources consumed by phyllostomids in the Pantanal wetland have phylogenetic signal, and that variation of the available vegetal resources influences the phylogenetic structure of phyllostomid assemblages. Considering the availability of their principal food resources, the two major phyllostomid clades (Phyllostominae and Stenodermatinae) responded in opposite ways to the vegetal resources gradient, formed by plant species with distinct adaptations to inundation. Our results indicate that the use of different habitats based on variation of vegetal resources is the main driver of phylogenetic structure of phyllostomid assemblages in the Pantanal wetland.
We examined both historical (1960s) and recent (2017) specimens of an insectivorous bat species (Hipposideros armiger) and a phytophagous bat (Rousettus leschenaultii) from the same latitudinal range to explore phenotypic responses to environmental change in China over the past 65 years. Hipposideros armiger exhibited significant increases in forearm length and three diet-related cranial traits, as well as carbon and nitrogen stable isotope composition, suggesting that modern H. armiger must travel farther for food and may now use different food resources. In contrast, R. leschenaultii showed no change in forearm length but displayed significant increases in diet-related cranial traits. This study provides evidence for differential responses to recent environmental changes in bat species with different diets. The changes in diet-related traits of the two species and the forearm length change on the insectivorous bats suggest that recent phenotypic changes may be adaptions to land-use changes rather than to climate change.
Interspecific competition affects population dynamics, distributional ranges, and evolution of competing species. The competitive exclusion principle states that ecologically similar species cannot coexist unless they exhibit niche segregation. Herein, we assess whether niche segregation allows the coexistence of Crocidura russula and C. suaveolens in southwestern Iberia and whether segregation is the result of current (ecological effect) or past (evolutionary effect) competition. We performed an annual live-trapping cycle in the two main habitats of the Odiel Marshes Natural Reserve (OMNR), the tidal marsh and the Mediterranean forest, both in syntopic (i.e., where both species co-occur) and allotopic (where only one of the two species occurs) sites within this Reserve. We modeled the presence–absence of each species in both habitats and sites by generalized linear mixed models. The coexistence of both species was favored by spatial and temporal niche segregation. Crocidura suaveolens was restricted to tidal marsh and did not occupy Mediterranean forest, even when C. russula was absent. We interpret this to be the result of competition in the past triggering an evolutionary response in C. suaveolens towards its specialization in tidal marsh. Moreover, the specialist C. suaveolens currently is outcompeting C. russula in tidal marshes, reversing the dominance pattern observed elsewhere. The degree of co-occurrence between both species in syntopic sites was low, as they showed inverse dynamics of seasonal abundances. Interspecific competition leading to habitat specialization favors the coexistence of these ecologically similar species.
Elevational gradients coincide with expansive climatic gradients and diverse plant and animal communities. We evaluated the small mammal assemblages in eight distinct vegetation types across an elevational gradient in southern California, the Deep Canyon Transect, to determine how assemblage composition changes across the gradient and to identify species with similar habitat associations. Livetrapping efforts (4,800 trap-nights) yielded 1,097 captures of 713 individuals, representing 14 heteromyid and cricetid species. Heteromyids dominated the six lower-elevation vegetation types (< 1,300 m a.s.l.), whereas cricetids dominated the upper end of the gradient. Richness and diversity exhibited bimodal responses to elevation, which do not conform to mid-domain effect null predictions. Canonical correspondence analysis revealed that 75% of the variation in small mammal abundances was explainable by habitat characteristics, and cluster analysis grouped small mammals into three ecologically distinct groups based on their habitat associations. One contained only Chaetodipus penicillatus, while the others were comprised of low- and high-elevation species, respectively. The low-elevation species exhibit unusual levels of sympatry (and syntopy) among closely related species of pocket mice (Chaetodipus). Further efforts should investigate the mechanisms of coexistence for Chaetodipus species with nearly identical associations and seasonal effects on richness and diversity. Repeated surveys of entire gradients such as the Deep Canyon Transect will help refine our understanding of temporal dynamics of community assemblage and diversity.
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