Reference genome of Townsend's big-eared bat, Corynorhinus townsendii.

Townsend's big-eared bat, Corynorhinus townsendii, is a cave- and mine-roosting species found largely in western North America. Considered a species of conservation concern throughout much of its range, protection efforts would greatly benefit from understanding patterns of population structure, genetic diversity, and local adaptation. To facilitate such research, we present the first de novo genome assembly of C. townsendii as part of the California Conservation Genomics Project (CCGP). Pacific Biosciences HiFi long reads and Omni-C chromatin-proximity sequencing technologies were used to produce a de novo genome assembly, consistent with the standard CCGP reference genome protocol. This assembly comprises 391 scaffolds spanning 2.1 Gb, represented by a scaffold N50 of 174.6 Mb, a contig N50 of 23.4 Mb, and a benchmarking universal single-copy ortholog (BUSCO) completeness score of 96.6%. This high-quality genome will be a key tool for informed conservation and management of this vulnerable species in California and across its range.

Predicting habitat suitability for Townsend's big-eared bats across California in relation to climate change.

Effective management decisions depend on knowledge of species distribution and habitat use. Maps generated from species distribution models are important in predicting previously unknown occurrences of protected species. However, if populations are seasonally dynamic or locally adapted, failing to consider population level differences could lead to erroneous determinations of occurrence probability and ineffective management. The study goal was to model the distribution of a species of special concern, Townsend's big-eared bats (Corynorhinus townsendii), in California. We incorporate seasonal and spatial differences to estimate the distribution under current and future climate conditions. We built species distribution models using all records from statewide roost surveys and by subsetting data to seasonal colonies, representing different phenological stages, and to Environmental Protection Agency Level III Ecoregions to understand how environmental needs vary based on these factors. We projected species' distribution for 2061-2080 in response to low and high emissions scenarios and calculated the expected range shifts. The estimated distribution differed between the combined (full dataset) and phenologically explicit models, while ecoregion-specific models were largely congruent with the combined model. Across the majority of models, precipitation was the most important variable predicting the presence of C. townsendii roosts. Under future climate scenarios, distribution of C. townsendii is expected to contract throughout the state, however suitable areas will expand within some ecoregions. Comparison of phenologically explicit models with combined models indicates the combined models better predict the extent of the known range of C. townsendii in California. However, life-history-explicit models aid in understanding of different environmental needs and distribution of their major phenological stages. Differences between ecoregion-specific and statewide predictions of habitat contractions highlight the need to consider regional variation when forecasting species' responses to climate change. These models can aid in directing seasonally explicit surveys and predicting regions most vulnerable under future climate conditions.

Variation in herpetofauna detection probabilities: implications for study design.

Population monitoring is fundamental for informing management decisions aimed at reducing the rapid rate of global biodiversity decline. Herpetofauna are experiencing declines worldwide and include species that are challenging to monitor. Raw counts and associated metrics such as richness indices are common for monitoring populations of herpetofauna; however, these methods are susceptible to bias as they fail to account for varying detection probabilities. Our goal was to develop a program for efficiently monitoring herpetofauna in southern Texas. Our objectives were to (1) estimate detection probabilities in an occupancy modeling framework using trap arrays for a diverse group of herpetofauna and (2) to evaluate the relative effectiveness of funnel traps, pitfall traps, and cover boards. We collected data with 36 arrays at 2 study sites in 2015 and 2016, for 2105 array-days resulting in 4839 detections of 51 species. We modeled occupancy for 21 species and found support for the hypothesis that detection probability varied over our sampling duration for 10 species and with rainfall for 10 species. For herpetofauna in our study, we found 14 and 12 species were most efficiently captured with funnel traps and pitfall traps, respectively, and no species were most efficiently captured with cover boards. Our results show that using methods that do not account for variations in detection probability are highly subject to bias unless the likelihood of false absences is minimized with exceptionally long capture durations. For monitoring herpetofauna in southern Texas, we recommend using arrays with funnel and pitfall traps and an analytical method such as occupancy modeling that accounts for variation in detection.

Secondhand homes: The multilayered influence of woodpeckers as ecosystem engineers.

Ecosystem engineers alter, and can be influenced in turn by, the ecosystems they live in. Woodpeckers choose foraging and nesting sites based, in part, on food availability. Once abandoned, these cavities, particularly within areas of high forage, may be crucial to secondary cavity-nesting birds otherwise limited by cavities formed through decay. Our study examined factors that influence the nesting success of primary cavity nesters and the subsequent impact on secondary cavity-nesting birds. Using 5 years of point count data, we monitored the outcomes of cavity-nesting birds in South Texas. We used logistic-exposure models to predict daily survival rates based on cavity metrics and used woodpecker foraging trends and insect surveys to determine if nesting where woodpeckers actively forage benefits secondary cavity-nesting birds. Both woodpeckers and secondary cavity nesters shared predictors of daily survival; nests were more successful in cavities with small openings in minimally decayed trees. All secondary cavity nesters had higher probabilities of success when nesting in an abandoned woodpecker cavity, opposed to ones formed by decay. Woodpeckers tended to forage in areas with higher-than-average levels of the insect orders Coleoptera, Hymenoptera, and Orthoptera, and secondary cavity nesters had higher rates of success when nesting in these areas. Our results suggest abandoned woodpecker cavities may be constructed in a way that directly benefit secondary cavity nesters. Additionally, we suggest an interplay between these ecosystem engineers, food availability, and secondary cavity nesters: Woodpeckers engineer superior nesting cavities in areas where food is more abundant, and the resultant cavities in areas of high forage may benefit local secondary cavity nesters. Our findings indicate that there is still much to be explored in the role of ecosystem engineers, and how they influence local communities on multiple trophic levels.

Ten-year projection of white-nose syndrome disease dynamics at the southern leading-edge of infection in North America.

Predicting the emergence and spread of infectious diseases is critical for the effective conservation of biodiversity. White-nose syndrome (WNS), an emerging infectious disease of bats, has resulted in high mortality in eastern North America. Because the fungal causative agent Pseudogymnoascus destructans is constrained by temperature and humidity, spread dynamics may vary by geography. Environmental conditions in the southern part of the continent are different than the northeast, where disease dynamics are typically studied, making it difficult to predict how the disease will manifest. Herein, we modelled WNS pathogen spread in Texas based on cave densities and average dispersal distances of hosts, projecting these results out to 10 years. We parameterized a predictive model of WNS epidemiology and its effects on bat populations with observed cave environmental data. Our model suggests that bat populations in northern Texas will be more affected by WNS mortality than southern Texas. As such, we recommend prioritizing the preservation of large overwintering colonies of bats in north Texas through management actions. Our model illustrates that infectious disease spread and infectious disease severity can become uncoupled over a gradient of environmental variation and highlight the importance of understanding host, pathogen and environmental conditions across a breadth of environments.

Factors Associated with Listing Decisions under the U.S. Endangered Species Act.

Conservation efforts, including authorities outlined in the U.S. Endangered Species Act (ESA) of 1973, are attempting to slow the decline of species. Opinions on the success of the ESA vary widely, due in part to few species historically recovering to the point of delisting. Uncertainty surrounding the ESA relates to listing decisions and ambiguity of terminology within the ESA itself. Our goal was to evaluate the relationship, if any, of species characteristics, population metrics, threat level, and potential non-biological indicators to listing decisions under the ESA by the U.S. Fish and Wildlife Service (Service). We collected data from 143 ESA listing decisions published in the Federal Register from February 2011 to October 2014. Only 33 and 31% of listing decisions included population or range size estimates, respectively. Factors significantly correlated with ESA listing decision included taxonomic group, primary ownership of the species' habitat (federal or non-federal), whether the species is aquatic or terrestrial, and whether the species was part of a single or multiple-species listing decision. Increasing number of listed threats and time as a candidate species correlated positively with being listed as endangered. We have attempted to broadly identify the role both intrinsic (biological) and extrinsic (non-biological) factors play in listing decisions, and the importance of comprehensive data to understanding species distribution and abundance to facilitate more informed listing decisions.

Iodine Redistribution During Trauma, Sepsis, and Hibernation: An Evolutionarily Conserved Response to Severe Stress.

OBJECTIVE: We performed these studies to learn how iodine in the form of free iodide behaves during stress. DESIGN: Prospective observational trial using samples obtained from human trauma patients and retrospective observational study using remnant samples from human sepsis patients and arctic ground squirrels. Preclinical interventional study using hind-limb ischemia and reperfusion injury in mice. SETTING: Level I trauma center emergency room and ICU and animal research laboratories. SUBJECTS: Adult human sepsis and trauma patients, wild-caught adult arctic ground squirrels, and sexually mature laboratory mice. INTERVENTIONS: Ischemia and reperfusion injury was induced in mice by temporary application of tourniquet to one hind-limb. Iodide was administered IV just prior to reperfusion. MEASUREMENTS AND MAIN RESULTS: Free iodide was measured using ion chromatography. Relative to iodide in plasma from normal donors, iodide was increased 17-fold in plasma from trauma patients and 26-fold in plasma from sepsis patients. In arctic ground squirrels, iodide increases over three-fold during hibernation. And during ischemia/reperfusion injury in mice, iodide accumulates in ischemic tissue and reduces both local and systemic tissue damage. CONCLUSIONS: Iodide redistributes during stress and improves outcome after injury. Essential functions of iodide may have contributed to its evolutionary selection and be useful as a therapeutic intervention for human patients.

Correction: Winter habitats of bats in Texas.

[This corrects the article DOI: 10.1371/journal.pone.0220839.].

Winter habitats of bats in Texas.

Few studies have described winter microclimate selection by bats in the southern United States. This is of particular importance as the cold-adapted fungus, Pseudogymnoascus destructans, which causes the fatal bat disease white-nose syndrome (WNS), continues to spread into southern United States. To better understand the suitability of winter bat habitats for the growth of P. destructans in this region, we collected roost temperature and vapor pressure deficit from 97 hibernacula in six ecoregions in Texas during winter 2016-17 and 2017-18. We also measured skin temperature of Rafinesque's big-eared bats (Corynorhinus townsendii), Townsend's big-eared bats (C. townsendii), big-brown bats (Eptesicus fuscus), southeastern myotis (Myotis austroriparius), cave myotis (M. velifer), tri-colored bats (Perimyotis subflavus), and Mexican free-tailed bats (Tadarida brasiliensis) during hibernation to study their use of torpor in these habitats. We found that temperatures within hibernacula were strongly correlated with external air temperatures and were often within the optimal range of temperatures for P. destructans growth. Hibernacula and skin temperatures differed among species, with Rafinesque's big-eared bats, southeastern myotis, and Mexican free-tailed bats occupying warmer microclimates and having higher torpid skin temperatures. For species that were broadly distributed throughout Texas, hibernacula and skin temperatures differed within species by ecoregion; Tri-colored bats and cave myotis in colder, northern regions occupied colder microclimates within hibernacula and exhibited colder skin temperatures, than individuals of the same species in warmer, southern regions. These data illustrate the variability in microclimates used as hibernacula by bats in Texas and suggest similar variation in susceptibility to WNS in the state. Thus, monitoring microclimates at winter roosts may help predict where WNS may develop, and where management efforts would be most effective.

External temperature and distance from nearest entrance influence microclimates of cave and culvert-roosting tri-colored bats (Perimyotis subflavus).

Many North American bat species hibernate in both natural and artificial roosts. Although hibernacula can have high internal climate stability, they still retain spatial variability in their thermal regimes, resulting in various "microclimates" throughout the roost that differ in their characteristics (e.g., temperature and air moisture). These microclimate components can be influenced by factors such as the number of entrances, the depth of the roost, and distance to the nearest entrance of the roost. Tri-colored bats are commonly found roosting in caves in winter, but they can also be found roosting in large numbers in culverts, providing the unique opportunity to investigate factors influencing microclimates of bats in both natural and artificial roost sites. As tri-colored bats are currently under consideration for federal listing, information of this type could be useful in aiding in the conservation and management of this species through a better understanding of what factors affect the microclimate near roosting bats. We collected data on microclimate temperature and microclimate actual water vapor pressure (AWVP) from a total of 760 overwintering tri-colored bats at 18 caves and 44 culverts. Using linear mixed models analysis, we found that variation in bat microclimate temperatures was best explained by external temperature and distance from nearest entrance in both caves and culverts. External temperature had a greater influence on microclimate temperatures in culverts than caves. We found that variation in microclimate AWVP was best explained by external temperature, distance from nearest entrance, and proportion from entrance (proportion of the total length of the roost from the nearest entrance) in culvert-roosting bats. Variation in microclimate AWVP was best explained by external temperature and proportion from entrance in cave-roosting bats. Our results suggest that bat microclimate temperature and AWVP are influenced by similar factors in both artificial and natural roosts, although the relative contribution of these factors differs between roost types.

A review of bat hibernacula across the western United States: Implications for white-nose syndrome surveillance and management.

Efforts to conserve bats in the western United States have long been impeded by a lack of information on their winter whereabouts, particularly bats in the genus Myotis. The recent arrival of white-nose syndrome in western North America has increased the urgency to characterize winter roost habitats in this region. We compiled 4,549 winter bat survey records from 2,888 unique structures across 11 western states. Myotis bats were reported from 18.5% of structures with 95% of aggregations composed of ≤10 individuals. Only 11 structures contained ≥100 Myotis individuals and 6 contained ≥500 individuals. Townsend's big-eared bat (Corynorhinus townsendii) were reported from 38% of structures, with 72% of aggregations composed of ≤10 individuals. Aggregations of ≥100 Townsend's big-eared bats were observed at 41 different caves or mines across 9 states. We used zero-inflated negative binomial regression to explore biogeographic patterns of winter roost counts. Myotis counts were greater in caves than mines, in more recent years, and in more easterly longitudes, northerly latitudes, higher elevations, and in areas with higher surface temperatures and lower precipitation. Townsend's big-eared bat counts were greater in caves, during more recent years, and in more westerly longitudes. Karst topography was associated with higher Townsend's big-eared bat counts but did not appear to influence Myotis counts. We found stable or slightly-increasing trends over time in counts for both Myotis and Townsend's big-eared bats from 82 hibernacula surveyed ≥5 winters since 1990. Highly-dispersed winter roosting of Myotis in the western USA complicates efforts to monitor population trends and impacts of disease. However, our results reveal opportunities to monitor winter population status of Townsend's big-eared bats across this region.

Iodide Improves Outcome After Acute Myocardial Infarction in Rats and Pigs.

OBJECTIVES: In this study, we tested whether iodide would reduce heart damage in rat and pig models of acute myocardial infarction as a risk analysis for a human trial. DESIGN: Prospective blinded and randomized laboratory animal investigation. SETTING: Animal research laboratories. SUBJECTS: Sexually mature rats and pigs. INTERVENTIONS: Acute myocardial infarction was induced by temporary ligation of the coronary artery followed by reperfusion. Iodide was administered orally in rats or IV in rats and pigs just prior to reperfusion. MEASUREMENTS AND MAIN RESULTS: Damage was assessed by blood cardiac troponin and infarct size; heart function was determined by echocardiography. Blood peroxide scavenging activity was measured enzymatically, and blood thyroid hormone was determined using radioimmune assay. Iodide administration preserved heart function and reduced blood cardiac troponin and infarct size by approximately 45% in pigs and approximately 60% in rats. Iodide administration also increased blood peroxide scavenging activity and maintained thyroid hormone levels. CONCLUSIONS: Iodide administration improved the structure and function of the heart after acute myocardial infarction in rats and pigs.

A before-after control-impact assessment to understand the potential impacts of highway construction noise and activity on an endangered songbird.

Anthropogenic noise associated with highway construction and operation can have individual- and population-level consequences for wildlife (e.g., reduced densities, decreased reproductive success, behavioral changes). We used a before-after control-impact study design to examine the potential impacts of highway construction and traffic noise on endangered golden-cheeked warblers (Setophaga chrysoparia; hereafter warbler) in urban Texas. We mapped and monitored warbler territories before (2009-2011), during (2012-2013), and after (2014) highway construction at three study sites: a treatment site exposed to highway construction and traffic noise, a control site exposed only to traffic noise, and a second control site exposed to neither highway construction or traffic noise. We measured noise levels at varying distances from the highway at sites exposed to construction and traffic noise. We examined how highway construction and traffic noise influenced warbler territory density, territory placement, productivity, and song characteristics. In addition, we conducted a playback experiment within study sites to evaluate acute behavioral responses to highway construction noises. Noise decreased with increasing distance from the highways. However, noise did not differ between the construction and traffic noise sites or across time. Warbler territory density increased over time at all study sites, and we found no differences in warbler territory placement, productivity, behavior, or song characteristics that we can attribute to highway construction or traffic noise. As such, we found no evidence to suggest that highway construction or traffic noise had a negative effect on warblers during our study. Because human population growth will require recurring improvements to transportation infrastructure, understanding wildlife responses to anthropogenic noise associated with the construction and operation of roads is essential for effective management and recovery of prioritized species.

Responses of a Federally Endangered Songbird to Understory Thinning in Oak-Juniper Woodlands.

Wildlife conservation and management on military lands must be accomplished in the context of military readiness, which often includes ground-based training that is perceived to conflict with wildlife needs and environmental regulations. From 2008‒2012, we examined territory density, pairing success, and fledging success of the federally endangered golden-cheeked warbler (Setophaga chrysoparia; hereafter warbler) in relation to removal of small-diameter trees from the understory of mature oak-juniper (Quercus-Juniperus) woodland at the 87,890 ha Fort Hood Military Reservation in central Texas. Understory thinning created troop maneuver lanes, but left canopy vegetation intact. Warbler density, pairing success, and fledging success were similar across thinned and control sites. We found that warbler pairing and fledging success were best predicted by Ecological site (hereafter Ecosite), an indicator of hardwood tree species composition. Warbler pairing and fledging success were about 1.5 and 1.6 times higher, respectively, for territories dominated by the Low Stony Hill Ecosite than territories dominated by the Redlands Ecosite. Our results indicate that understory thinning for military training purposes did not have a negative effect on warblers at Fort Hood in the manner tested, and suggest that removal of smaller trees from the understory in a way that replicates historic conditions may elicit neutral responses from this forest-dependent songbird. Quantifying wildlife responses to military activities provides the Department of Defense and US Fish and Wildlife Service with data to guide conservation of threatened and endangered species on Department of Defense facilities while maintaining the military mission, and supports wildlife management efforts on other public and private lands.

Selenide Targets to Reperfusing Tissue and Protects It From Injury.

OBJECTIVES: Since blood selenium levels decrease after ischemia and reperfusion injury, and low blood selenium correlates with negative outcome, we designed and performed experiments to determine how selenium distribution is affected by ischemia reperfusion injury. Furthermore, we tested whether different chemical forms of selenium would affect outcome after ischemia and reperfusion injury. We also examined the metabolic effects of selenide administration. DESIGN: Laboratory investigation. SETTING: Animal research laboratory. SUBJECTS: Adult male C57BL/6 mice. INTERVENTIONS: To determine selenium localization, we administered tracer doses of radioactive selenium 75 in the form of selenite or selenide and measured blood and tissue selenium levels after ischemia and reperfusion injury. Anesthetized mice were subjected to myocardial ischemia reperfusion injury (coronary artery occlusion for 60 min followed by 5 min of reperfusion after occlusion was removed) or hindlimb ischemia reperfusion injury (left leg tourniquet for 90 min followed by 5 min reperfusion after tourniquet removal). To determine whether exogenous selenium administration could reduce ischemia reperfusion injury, we synthesized and administered sodium hydroselenide and sodium selenite solutions (0.05-2.4 mg/kg). Solutions were administered at the end of coronary artery occlusion but before reperfusion. In order to determine the metabolic effects of selenide administration, we exposed mice to hydrogen selenide gas (0-5 ppm) mixed into air (20.95% oxygen) for up to 3 hours. MEASUREMENTS AND MAIN RESULTS: In targeting assays, we measured blood and tissue selenium levels. We observed that blood selenium decreases after myocardial ischemia reperfusion and displays an inverse correlation with injury severity; selenium accumulation in heart correlates directly with injury severity. We also measured whether oxidized selenium, selenite, and reduced selenium, selenide, would target to injured heart tissue in myocardial ischemia reperfusion and injured leg muscle in a hindlimb model of ischemia reperfusion. Only selenide targets to injured tissue. We also measured damage after myocardial ischemia reperfusion injury using morphometry, neutrophil accumulation, blood cardiac troponin levels, and echocardiography and observed in all assays that selenide reduced damage to the heart; selenite was not effective. And finally, to assay metabolism, we measured oxygen consumption, carbon dioxide production, and body core temperature before, during, and after hydrogen selenide administration. All measurements indicate that selenide decreases metabolism. CONCLUSIONS: Selenide targets to reperfusing tissue and reduces reperfusion injury perhaps by affecting oxygen metabolism.

Iodide protects heart tissue from reperfusion injury.

Iodine is an elemental nutrient that is essential for mammals. Here we provide evidence for an acute therapeutic role for iodine in ischemia reperfusion injury. Infusion of the reduced form, iodide, but not the oxidized form iodate, reduces heart damage by as much as 75% when delivered intravenously following temporary loss of blood flow but prior to reperfusion of the heart in a mouse model of acute myocardial infarction. Normal thyroid function may be required because loss of thyroid activity abrogates the iodide benefit. Given the high degree of protection and the high degree of safety, iodide should be explored further as a therapy for reperfusion injury.

Breeding phenology of birds: mechanisms underlying seasonal declines in the risk of nest predation.

Seasonal declines in avian clutch size are well documented, but seasonal variation in other reproductive parameters has received less attention. For example, the probability of complete brood mortality typically explains much of the variation in reproductive success and often varies seasonally, but we know little about the underlying cause of that variation. This oversight is surprising given that nest predation influences many other life-history traits and varies throughout the breeding season in many songbirds. To determine the underlying causes of observed seasonal decreases in risk of nest predation, we modeled nest predation of Dusky Flycatchers (Empidonax oberholseri) in northern California as a function of foliage phenology, energetic demand, developmental stage, conspecific nest density, food availability for nest predators, and nest predator abundance. Seasonal variation in the risk of nest predation was not associated with seasonal changes in energetic demand, conspecific nest density, or predator abundance. Instead, seasonal variation in the risk of nest predation was associated with foliage density (early, but not late, in the breeding season) and seasonal changes in food available to nest predators. Supplemental food provided to nest predators resulted in a numerical response by nest predators, increasing the risk of nest predation at nests that were near supplemental feeders. Our results suggest that seasonal changes in foliage density and factors associated with changes in food availability for nest predators are important drivers of temporal patterns in risk of avian nest predation.

Conspecific cues and breeding habitat selection in an endangered woodland warbler.

1. Research on habitat selection has focused on the role of vegetative and geologic characteristics or antagonistic behavioural interactions. 2. Conspecifics can confer information about habitat quality and provide positive density-dependent effects, suggesting habitat selection in response to the presence of conspecifics can be an adaptive strategy. 3. We conducted a manipulative field experiment investigating use of conspecific location cues for habitat selection and consequent reproductive outcomes for the endangered golden-cheeked warbler (Setophaga chrysoparia). We investigated the response in woodlands across a range of habitat canopy cover conditions typically considered suitable to unsuitable and using vocal cues presented during two time periods: pre-settlement and post-breeding. 4. Warblers showed a strong response to both pre-settlement and post-breeding conspecific cues. Territory density was greater than four times higher in treatment sample units than controls. The magnitude of response was higher for cues presented during the pre-settlement period. Positive response to conspecific cues was consistent even in previously unoccupied areas with low canopy cover typically considered unsuitable, resulting in aggregations of warblers in areas generally not considered potential habitat. 5. Pairing and reproductive success of males was not correlated with canopy cover, as commonly thought. Pairing success and fledging success increased with increasing territory density suggesting that conspecific density may be more important for habitat selection decisions than the canopy cover conditions typically thought to be most important. These results suggest the range of habitat within which birds can perform successfully may be greater than is typically observed. 6. Our results suggest the territory selection process may not be substantially influenced by competition in some systems. Settlement in response to conspecific cues produced aggregations within larger areas of similar vegetative characteristics. Understanding what cues drive habitat selection decisions and whether these cues are correlated with habitat quality is critical for conserving fitness-enhancing habitats, avoiding creation of ecological traps, generating accurate predictions of species distributions and understanding how occupancy relates to habitat suitability.