Long-term spring through fall capture data of Eptesicus fuscus in the eastern USA before and after white-nose syndrome.

Emerging infectious diseases threaten wildlife populations. Without well monitored wildlife systems, it is challenging to determine accurate population and ecosystem losses following disease emergence. North American temperate bats present a unique opportunity for studying the broad impacts of wildlife disease emergence, as their federal monitoring programs were prioritized in the USA throughout the 20th century and they are currently threatened by the invasive fungal pathogen, Pseudogymnoascus destructans (Pd), which causes white-nose syndrome. Here we provide a long-term dataset for capture records of Eptesicus fuscus (big brown bat) across the eastern USA, spanning 16 years before and 14 years after Pd invasion into North America. These data represent 30,496 E. fuscus captures across 3,567 unique sites. We encourage the use of this dataset for quantifying impacts of wildlife disease and other threats to wildlife (e.g., climate change) with the incorporation of other available data. We welcome additional data contributions for E. fuscus captures across North and Central America as well as the inclusion of other variables into the dataset that contribute to the quantification of wildlife health.

A low-density single nucleotide polymorphism panel for brown trout (Salmo trutta L.) suitable for exploring genetic diversity at a range of spatial scales.

The rivers of southern England and northern France which drain into the English Channel contain several genetically unique groups of trout (Salmo trutta L.) that have suffered dramatic declines in numbers over the past 40 years. Knowledge of levels and patterns of genetic diversity is essential for effective management of these vulnerable populations. Using restriction site-associated DNA sequencing (RADseq) data, we describe the development and characterisation of a panel of 95 single nucleotide polymorphism (SNP) loci for trout from this region and investigate their applicability and variability in both target (i.e., southern English) and non-target trout populations from northern Britain and Ireland. In addition, we present three case studies which demonstrate the utility and resolution of these genetic markers at three levels of spatial separation:(a) between closely related populations in nearby rivers, (b) within a catchment and (c) when determining parentage and familial relationships between fish sampled from a single site, using both empirical and simulated data. The SNP loci will be useful for population genetic and assignment studies on brown trout within the UK and beyond.

The scope and severity of white-nose syndrome on hibernating bats in North America.

Assessing the scope and severity of threats is necessary for evaluating impacts on populations to inform conservation planning. Quantitative threat assessment often requires monitoring programs that provide reliable data over relevant spatial and temporal scales, yet such programs can be difficult to justify until there is an apparent stressor. Leveraging efforts of wildlife management agencies to record winter counts of hibernating bats, we collated data for 5 species from over 200 sites across 27 U.S. states and 2 Canadian provinces from 1995 to 2018 to determine the impact of white-nose syndrome (WNS), a deadly disease of hibernating bats. We estimated declines of winter counts of bat colonies at sites where the invasive fungus that causes WNS (Pseudogymnoascus destructans) had been detected to assess the threat impact of WNS. Three species undergoing species status assessment by the U.S. Fish and Wildlife Service (Myotis septentrionalis, Myotis lucifugus, and Perimyotis subflavus) declined by more than 90%, which warrants classifying the severity of the WNS threat as extreme based on criteria used by NatureServe. The scope of the WNS threat as defined by NatureServe criteria was large (36% of Myotis lucifugus range) to pervasive (79% of Myotis septentrionalis range) for these species. Declines for 2 other species (Myotis sodalis and Eptesicus fuscus) were less severe but still qualified as moderate to serious based on NatureServe criteria. Data-sharing across jurisdictions provided a comprehensive evaluation of scope and severity of the threat of WNS and indicated regional differences that can inform response efforts at international, national, and state or provincial jurisdictions. We assessed the threat impact of an emerging infectious disease by uniting monitoring efforts across jurisdictional boundaries and demonstrated the importance of coordinated monitoring programs, such as the North American Bat Monitoring Program (NABat), for data-driven conservation assessments and planning.

Alcance y Severidad del Síndrome de Nariz Blanca en los Murciélagos Hibernando en América del Norte Resumen La evaluación del alcance y la severidad de las amenazas es necesaria para los análisis de impacto sobre las poblaciones que se usan para orientar a la planeación de la conservación. La evaluación cuantitativa de amenazas con frecuencia requiere de programas de monitoreo que proporcionen datos confiables en escalas espaciales y temporales, aunque dichos programas pueden ser difíciles de justificar hasta que exista un estresante aparente. Gracias a una movilización de esfuerzos de las agencias de manejo de fauna para registrar los conteos invernales de murciélagos hibernadores, recopilamos datos para cinco especies en más de 200 sitios a lo largos de 27 estados de EUA y dos provincias canadienses entre 1995 y 2018 para determinar el impacto del síndrome de nariz blanca (SNB), una enfermedad mortal de los murciélagos hibernadores. Estimamos declinaciones en los conteos invernales de las colonias de murciélagos en sitios en donde el hongo invasivo que ocasiona el SNB (Pseudogymnoascus destructans) había sido detectado para evaluar el impacto de amenaza del SNB. Tres especies que se encuentran bajo valoración por parte del Servicio de Pesca y Vida Silvestre de los EUA (Myotis septentrionalis, Myotis lucifugus y Perimyotis subflavus) tuvieron una declinación de más del 90%, lo que justifica la clasificación de la severidad de la amenaza del SNB como extrema con base en el criterio usado por NatureServe. El alcance de la amenaza del SNB definido por el criterio de NatureServe fue desde amplio (36% de la distribución de Myotis lucifugus) hasta dominante (79% de la distribución de Myotis septentrionalis) para estas especies. Las declinaciones de otras dos especies (Myotis sodalis y Eptesicus fuscus) fueron menos severas, pero de igual manera quedaron clasificadas desde moderada hasta seria con base en los criterios de NatureServe. El intercambio de datos entre las jurisdicciones proporcionó una evaluación completa del alcance y la severidad de la amenaza del SNB e indicó las diferencias regionales que pueden guiar a los esfuerzos de respuesta realizados en las jurisdicciones internacionales, nacionales, estatales o provinciales. Evaluamos el impacto de amenaza de una enfermedad infecciosa emergente mediante la combinación de los esfuerzos de monitoreo que sobrepasan fronteras jurisdiccionales y demostramos la importancia que tienen para la planeación y la evaluación basadas en datos de la conservación los programas de monitoreo coordinados, como el Programa de Monitoreo de los Murciélagos Norteamericanos (NABat).

Small coastal streams-Critical reservoirs of genetic diversity for trout (Salmo trutta L.) in the face of increasing anthropogenic stressors.

We used microsatellite markers to investigate levels and structuring of genetic diversity in trout (Salmo trutta L.) sampled from 16 rivers along the south coast of Cornwall in southwest England. This region is characterized by many small coastal streams with a few larger catchments. At a regional level, genetic structuring of contemporary populations has been influenced by a combination of events, including the last Ice Age and also more recent human activities over the last millennium. All populations are shown to have gone through strong genetic bottlenecks, coinciding with increased exploitation of mineral resources within catchments, beginning during the Medieval period. At more local levels, contemporary human-induced habitat fragmentation, such as weir and culvert construction, has disproportionally affected trout populations in the smaller catchments within the study area. However, where small catchments are relatively unaffected by such activities, they can host trout populations with diversity levels comparable to those found in larger rivers in the region. We also predict significant future loses of diversity and heterozygosity in the trout populations inhabiting small, isolated catchments. Our study highlights how multiple factors, especially the activity of humans, have and continue to affect the levels and structuring of genetic diversity in trout over long timescales.

Apomixis and Hybridization Drives Reticulate Evolution and Phyletic Differentiation in Sorbus L.: Implications for Conservation.

Hybridization and polyploidy are major forces in the evolution of plant diversity and the study of these processes is of particular interest to understand how novel taxa are formed and how they maintain genetic integrity. Sorbus is an example of a genus where active diversification and speciation are ongoing and, as such, represents an ideal model to investigate the roles of hybridization, polyploidy and apomixis in a reticulate evolutionary process. To elucidate breeding systems and evolutionary origins of a complex of closely related Sorbus taxa, we assessed genotypic diversity and population structure within and among taxa, combining data from nuclear DNA microsatellite markers and flow cytometry. Clonal analysis and low genotypic diversity within the polyploid taxa suggest apomixis is obligate. However, genetic variation has led to groups of 'clone-mates' within apomictic taxa that strongly suggest mutation is responsible for the genotypic diversity of these apomictic lineages. In addition, microsatellite profiles and site demographics suggest hybridization events among apomictic polyploid Sorbus may have contributed to the extant diversity of recognized taxa in this region. This research demonstrates that both macro- and micro-evolutionary processes are active within this reticulate Sorbus complex. Conservation measures should be aimed at maintaining this process and should therefore be prioritized for those areas of Sorbus species richness where the potential for interspecific gene flow is greatest.

Human mining activity across the ages determines the genetic structure of modern brown trout (Salmo trutta L.) populations.

Humans have exploited the earth's metal resources for thousands of years leaving behind a legacy of toxic metal contamination and poor water quality. The southwest of England provides a well-defined example, with a rich history of metal mining dating to the Bronze Age. Mine water washout continues to negatively impact water quality across the region where brown trout (Salmo trutta L.) populations exist in both metal-impacted and relatively clean rivers. We used microsatellites to assess the genetic impact of mining practices on trout populations in this region. Our analyses demonstrated that metal-impacted trout populations have low genetic diversity and have experienced severe population declines. Metal-river trout populations are genetically distinct from clean-river populations, and also from one another, despite being geographically proximate. Using approximate Bayesian computation (ABC), we dated the origins of these genetic patterns to periods of intensive mining activity. The historical split of contemporary metal-impacted populations from clean-river fish dated to the Medieval period. Moreover, we observed two distinct genetic populations of trout within a single catchment and dated their divergence to the Industrial Revolution. Our investigation thus provides an evaluation of contemporary population genetics in showing how human-altered landscapes can change the genetic makeup of a species.

Molecular evidence for gender differences in the migratory behaviour of a small seabird.

Molecular sexing revealed an unexpectedly strong female bias in the sex ratio of pre-breeding European Storm Petrels (Hydrobates pelagicus), attracted to playback of conspecific calls during their northwards migration past SW Europe. This bias was consistent across seven years, ranging from 80.8% to 89.7% female (mean annual sex ratio ± SD = 85.5% female ±4.1%). The sex ratio did not differ significantly from unity (i.e., 50% female) among (i) Storm Petrel chicks at a breeding colony in NW France, (ii) adults found dead on beaches in Southern Portugal, (iii) breeding birds attending nest burrows in the UK, captured by hand, and (iv) adults captured near a breeding colony in the UK using copies of the same sound recordings as used in Southern Europe, indicating that females are not inherently more strongly attracted to playback calls than males. A morphological discriminant function analysis failed to provide a good separation of the sexes, showing the importance of molecular sexing for this species. We found no sex difference in the seasonal or nocturnal timing of migration past Southern Europe, but there was a significant tendency for birds to be caught in sex-specific aggregations. The preponderance of females captured in Southern Europe suggests that the sexes may differ in migration route or in their colony-prospecting behaviour during migration, at sites far away from their natal colonies. Such differences in migration behaviour between males and females are poorly understood but have implications for the vulnerability of seabirds to pollution and environmental change at sea during the non-breeding season.

Space-time models for a panzootic in bats, with a focus on the endangered Indiana bat.

Knowledge of current trends of quickly spreading infectious wildlife diseases is vital to efficient and effective management. We developed space-time mixed-effects logistic regressions to characterize a disease, white-nose syndrome (WNS), quickly spreading among endangered Indiana bats (Myotis sodalis) in eastern North America. Our goal was to calculate and map the risk probability faced by uninfected colonies of hibernating Indiana bats. Model covariates included annual distance from and direction to nearest sources of infection, geolocational information, size of the Indiana bat populations within each wintering population, and total annual size of populations known or suspected to be affected by WNS. We considered temporal, spatial, and spatiotemporal formulae through the use of random effects for year, complex (a collection of interacting hibernacula), and year × complex. Since first documented in 2006, WNS has spread across much of the range of the Indiana bat. No sizeable wintering population now occurs outside of the migrational distance of an infected source. Annual rates of newly affected wintering Indiana bat populations between winter 2007 to 2008 and 2010 to 2011 were 4, 6, 8, and 12%; this rate increased each year at a rate of 3%. If this increasing rate of newly affected populations continues, all wintering populations may be affected by 2016. Our models indicated the probability of a wintering population exhibiting infection was a linear function of proximity to affected Indiana bat populations and size of the at-risk population. Geographic location was also important, suggesting broad-scale influences. For every 50-km increase in distance from a WNS-affected population, risk of disease declined by 6% (95% CI=5.2-5.7%); for every increase of 1,000 Indiana bats, there was an 8% (95% CI = 1-21%) increase in disease risk. The increasing rate of infection seems to be associated with the movement of this disease into the core of the Indiana bat range. Our spatially explicit estimates of disease risk may aid managers in prioritizing surveillance and management for wintering populations of Indiana bats and help understand the risk faced by other hibernating bat species.

Molecular diagnostics reveal spiders that exploit prey vibrational signals used in sexual communication.

Vibrational signalling is a widespread form of animal communication and, in the form of sexual communication, has been generally regarded as inherently short-range and a private communication channel, free from eavesdropping by generalist predators. A combination of fieldwork and laboratory experiments was used to test the hypothesis that predators can intercept and exploit such signals. First, we developed and characterized PCR primers specific for leafhoppers of the genus Aphrodes and specifically for the species Aphrodes makarovi. Spiders were collected from sites where leafhoppers were present and screened with these primers to establish which spider species were significant predators of this species during the mating period of these leafhoppers. Analysis using PCR of the gut contents of tangle-web spiders, Enoplognatha ovata (Theridiidae), showed that they consume leafhoppers in the field at a greater rate when signalling adults were present than when nymphs were dominant, suggesting that the spiders were using these vibrations signals to find their prey. Playback and microcosm experiments then showed that E. ovata can use the vibrational signals of male leafhoppers as a cue during foraging and, as a result, killed significantly more male than female A. makarovi. Our results show, for the first time, that arthropod predators can exploit prey vibrational communication to obtain information about prey availability and use this information to locate and capture prey. This may be a widespread mechanism for prey location, one that is likely to be a major unrecognized driver of evolution in both predators and prey.

Multiplex reactions for the molecular detection of predation on pest and nonpest invertebrates in agroecosystems.

Species- and group-specific PCR primers were developed to study predation on pest and nonpest invertebrate species by generalist carabid predators in agroecosystems. To ensure the amplification of degraded DNA in predator gut samples, amplicons were designed to be less than 300 bp. Specificity of primers was assessed by cross-amplification against a panel of target and nontarget invertebrate species. The new primers were combined with previously published primers for slugs and collembolla in multiplex reactions to simultaneously screen each predator for the presence of multiple prey. All prey species were detected in a screen of the gut contents of field-caught predators.

Prey choice by carabid beetles feeding on an earthworm community analysed using species- and lineage-specific PCR primers.

The carabid beetle Pterostichus melanarius is a major natural enemy of pests, such as aphids and slugs in agricultural systems. Earthworms are a dominant non-pest component of the diet of P. melanarius which help sustain the beetles during periods when the pest population is low or absent. In this study we wanted to test whether this predator exercises prey choice among different earthworm species or ecological groups. High levels of genetic diversity within morphological species of earthworm necessitated the development of primers that were specific not just to species but lineages and sub-lineages within species as well. Gut samples from beetles were analysed using multiplex-PCR and fluorescent-labelled primers. Calibratory feeding trials were undertaken to calculate median detection times for prey DNA following ingestion. Extensive testing demonstrated that the primers were species-specific, that detection periods were negatively related to amplicon size and that meal size had a highly significant effect on detection periods. Monte Carlo simulations showed that, in general, worms were being predated in proportion to their densities in the field with little evidence of prey choice, other than probable avoidance of the larger, deep-living species. There was no evidence that epigeic species were being taken preferentially in comparison with endogeic species. There was also no evidence that defensive secretions by Allolobophora chlorotica reduced predation pressure on this species by P. melanarius. We concluded that any management system that increases earthworm densities generally, regardless of component species, is likely to be optimal for increasing numbers of this beneficial beetle predator.

Opening a can of worms: unprecedented sympatric cryptic diversity within British lumbricid earthworms.

Earthworms play a major role in many aspects of soil fertility, food web ecology and ecosystem functioning, and hence are frequently the subjects of, for example, ecological and toxicological research. Our aim was to examine the genetic structure of common earthworm species, to identify cryptic lineages or species that may be distinct ecotypes or biotypes (and hence confound current research based upon morphotypes) and to try to explain the massive cryptic diversity that eventually emerged. We demonstrated that species such as Allolobophora chlorotica, Aporrectodea longa, Aporrectodea rosea and Lumbricus rubellus all comprise highly divergent lineages with species-level divergence at the mitochondrial cytochrome oxidase I (COI) gene. In Allo. chlorotica alone, we found 55 haplotypes for COI, with 35 of these being found in pink and 20 in green morph worms. There were no cases of the two colour morphs sharing COI haplotypes. Phylogenetic analyses of mitochondrial COI and 16S genes showed the presence of five highly divergent lineages, suggesting the presence of multiple cryptic species within Allo. chlorotica. There was no clear geographical pattern to lineage distribution and many populations were polymorphic for both mitochondrial DNA lineage and colour morph. Amplified fragment length polymorphism results, based on two primer combinations, were broadly congruent with mitochondrial DNA results with one significant exception. Despite showing over 14% divergence at COI, amplified fragment length polymorphism markers showed that the two green morph lineages may be interbreeding and therefore represent a single taxon. The cryptic diversity revealed by these results has profound consequences for all areas of earthworm research.

A variable minisatellite sequence in the chloroplast genome of Sorbus L. (Rosaceae: Maloideae).

The chloroplast genome is now known to be more variable than was once thought. Reports of RFLP (restriction fragment length polymorphism) and sequence variation, as well as variation in chloroplast microsatellites, are common. Here, data are presented on the variability of a minisatellite sequence in the chloroplast genome of Sorbus species. RFLP analysis of a PCR product comprising the region between the trnM and rbcL genes of nine Sorbus species identified seven size variants. Sequencing revealed the observed size polymorphism to be due to differences in the number of copies of an imperfect 9-bp motif. A more intensive survey of the variability of the minisatellite was undertaken in populations of Sorbus aucuparia. The potential uses of such regions in chloroplast DNA are discussed and a possible mechanism for the evolution of the minisatellite is presented.