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Application of genetics and genomics to wildlife epidemiology

Wildlife diseases can have significant impacts on wildlife conservation and management. Many of the pathogens that affect wildlife also have important implications for domestic animal and human health. However, management interventions to prevent or control wildlife disease are hampered by uncertainties about the complex interactions between pathogens and free-ranging wildlife. We often lack crucial knowledge about host ecology, pathogen characteristics, and host–pathogen dynamics. The purpose of this review is to familiarize wildlife biologists and managers with the application of genetic and genomic methodologies for investigating pathogen and host biology to better understand and manage wildlife diseases. The genesis of this review was a symposium at the 2013 annual Wildlife Society Conference. We reviewed the scientific literature and used our personal experiences to identify studies that illustrate the application of genetic and genomic methods to advance our understanding of wildlife epidemiology, focusing on recent research, new techniques, and innovative approaches. Using examples from a variety of pathogen types and a broad array of vertebrate taxa, we describe how genetics and genomics can provide tools to detect and characterize pathogens, uncover routes of disease transmission and spread, shed light on the ways that disease susceptibility is influenced by both host and pathogen attributes, and elucidate the impacts of disease on wildlife populations. Genetic and increasingly genomic methodologies will continue to contribute important insights into pathogen and host biology that will aid efforts to assess and mitigate the impacts of wildlife diseases on global health and conservation of biodiversity.

Journal of Wildlife Management

Trout in hot water: A call for global action

Trout are one of the most culturally, economically, and ecologically important taxonomic groups of freshwater fishes worldwide (1). Native to all continents in the Northern Hemisphere, trout are a taxonomically diverse group of fishes belonging to 7 genera (Oncorhynchus, Salvelinus, Salmo, Hucho, Parahucho, Brachymystax, and Salvethymus) distributed across 52 countries. These coldwater specialists provide recreation and food to millions of people, and play important roles in ecosystem functioning and health (2). They are also extremely sensitive to human disturbances because they require cold, clean, complex, and connected habitats for survival and persistence (3) – all attributes that humans have substantially altered and degraded (4, 5). Despite their broad importance as societal icons and as indicators of biodiversity, many of the world’s trout species and lineages are endangered and some require immediate conservation efforts to reverse their precarious decline.

Science

Establishing the foundation for the global observing system for marine life

Maintaining healthy, productive ecosystems in the face of pervasive and accelerating human impacts including climate change requires globally coordinated and sustained observations of marine biodiversity. Global coordination is predicated on an understanding of the scope and capacity of existing monitoring programs, and the extent to which they use standardized, interoperable practices for data management. Global coordination also requires identification of gaps in spatial and ecosystem coverage, and how these gaps correspond to management priorities and information needs. We undertook such an assessment by conducting an audit and gap analysis from global databases and structured surveys of experts. Of 371 survey respondents, 203 active, long-term (>5 years) observing programs systematically sampled marine life. These programs spanned about 7% of the ocean surface area, mostly concentrated in coastal regions of the United States, Canada, Europe, and Australia. Seagrasses, mangroves, hard corals, and macroalgae were sampled in 6% of the entire global coastal zone. Two-thirds of all observing programs offered accessible data, but methods and conditions for access were highly variable. Our assessment indicates that the global observing system is largely uncoordinated which results in a failure to deliver critical information required for informed decision-making such as, status and trends, for the conservation and sustainability of marine ecosystems and provision of ecosystem services. Based on our study, we suggest four key steps that can increase the sustainability, connectivity and spatial coverage of biological Essential Ocean Variables in the global ocean: (1) sustaining existing observing programs and encouraging coordination among these; (2) continuing to strive for data strategies that follow FAIR principles (findable, accessible, interoperable, and reusable); (3) utilizing existing ocean observing platforms and enhancing support to expand observing along coasts of developing countries, in deep ocean basins, and near the poles; and (4) targeting capacity building efforts. Following these suggestions could help create a coordinated marine biodiversity observing system enabling ecological forecasting and better planning for a sustainable use of ocean resources.

Frontiers in Marine Science

Misleading prioritizations from modelling range shifts under climate change

Aim Conservation planning requires the prioritization of a subset of taxa and geographical locations to focus monitoring and management efforts. Integration of the threats and opportunities posed by climate change often relies on predictions from species distribution models, particularly for assessments of vulnerability or invasion risk for multiple taxa. We evaluated whether species distribution models could reliably rank changes in species range size under climate and land use change. Location Conterminous U.S.A. Time period 1977–2014. Major taxa studied Passerine birds. Methods We estimated ensembles of species distribution models based on historical North American Breeding Bird Survey occurrences for 190 songbirds, and generated predictions to recent years given c . 35 years of observed land use and climate change. We evaluated model predictions using standard metrics of discrimination performance and a more detailed assessment of the ability of models to rank species vulnerability to climate change based on predicted range loss, range gain, and overall change in range size. Results Species distribution models yielded unreliable and misleading assessments of relative vulnerability to climate and land use change. Models could not accurately predict range expansion or contraction, and therefore failed to anticipate patterns of range change among species. These failures occurred despite excellent overall discrimination ability and transferability to the validation time period, which reflected strong performance at the majority of locations that were either always or never occupied by each species. Main conclusions Models failed for the questions and at the locations of greatest interest to conservation and management. This highlights potential pitfalls of multi-taxa impact assessments under global change; in our case, models provided misleading rankings of the most impacted species, and spatial information about range changes was not credible. As modelling methods and frameworks continue to be refined, performance assessments and validation efforts should focus on the measures of risk and vulnerability useful for decision-making.

Global Ecology and Biogeography

The Southwestern Pond Turtle (Actinemys pallida) in Baja California, Mexico: New localities and persistent threats

The Southwestern Pond Turtle ( Actinemys pallida ), the only native freshwater turtle in Baja California, is experiencing alarming population declines, echoing global patterns observed in freshwater turtles. We conducted comprehensive field surveys across the major drainages of northwestern Baja California to delineate the species' current distribution, identify critical threats to its persistence, and provide guidance for conservation actions. We documented the continued presence of A. pallida at 27 sites across 10 watersheds, ranging from sea level to 1,525 m in elevation. These include nine historically known sites and 18 newly recorded localities. The most pervasive threats we identified were habitat degradation, the proliferation of invasive aquatic species, and unsustainable water extraction. Despite these pressures, our findings confirm that A. pallida still occupies much of its historical range. However, urgent ecological research is needed to inform evidence-based strategies that ensure the long-term viability of this imperiled species.

Baja California

Developing multi-model ensemble projections of ecologically relevant climate variables for Puerto Rico and the US Caribbean

The global increases in surface air temperature are the most widespread and direct consequence of anthropogenic climate change. However, while 21st century temperatures are projected to increase in the Caribbean, the low variability and high average temperatures suggest that impacts on ecosystems and water resources are more likely through changes to the availability, timing, and pattern of moisture. The lack of local-scale climate model information that can resolve the complex topography and small scale climate features hinders the development of robust adaptation strategies. The goal of this project was to develop a suite of local-scale climate projections using dynamic downscaling to aid the development of adaptation strategies in Puerto Rico and the U.S. Virgin Islands (USVI). This project began by engaging the ecologists, hydrologists, and conservation biologists in the region to determine the most valuable types of information to aid research and decision making. The final product provides projections of future climate at a 2km horizontal resolution based on three global climate models and two regional climate models for a scenario with high greenhouse gas emissions. Results from the projections suggest that for Puerto Rico, annual temperature would increase between 1°C and 1.3°C by mid-century with larger temperature increases located in the interior portion of the island. Precipitation totals decrease for much of the island with island average decline between 12% and 19%, with some potentially large localized decreases exceeding 30%. The projected changes for the USVI are dominated by the surrounding ocean environment. The resulting projections will be provided to stakeholders in the region via the USGS and the CLCC.

Puerto Rico

Impacts of climatic variation on trout: A global synthesis and path forward

Despite increasing concern that climate change may negatively impact trout—a globally distributed group of fish with major economic, ecological, and cultural value—a synthetic assessment of empirical data quantifying relationships between climatic variation and trout ecology does not exist. We conducted a systematic review to describe how temporal variation in temperature and streamflow influences trout ecology in freshwater ecosystems. Few studies ( n = 42) have quantified relationships between temperature or streamflow and trout demography, growth, or phenology, and nearly all estimates (96 %) were for Salvelinus fontinalis and Salmo trutta . Only seven studies used temporal data to quantify climate-driven changes in trout ecology. Results from these studies were beset with limitations that prohibited quantitatively rigorous meta-analysis, a concerning inadequacy given major investment in trout conservation and management worldwide. Nevertheless, consistent patterns emerged from our synthesis, particularly a positive effect of summer streamflow on trout demography and growth; 64 % of estimates were positive and significant across studies, age classes, species, and locations, highlighting that climate-induced changes in hydrology may have numerous consequences for trout. To a lesser degree, summer and fall temperatures were negatively related to population demography (51 and 53 % of estimates, respectively), but temperature was rarely related to growth. To address limitations and uncertainties, we recommend: (1) systematically improving data collection, description, and sharing; (2) appropriately integrating climate impacts with other intrinsic and extrinsic drivers over the entire lifecycle; (3) describing indirect consequences of climate change; and (4) acknowledging and describing intrinsic resiliency.

Reviews in Fish Biology and Fisheries

Species and population specific gene expression in blood transcriptomes of marine turtles

Background Transcriptomic data has demonstrated utility to advance the study of physiological diversity and organisms’ responses to environmental stressors. However, a lack of genomic resources and challenges associated with collecting high-quality RNA can limit its application for many wild populations. Minimally invasive blood sampling combined with de novo transcriptomic approaches has great potential to alleviate these barriers. Here, we advance these goals for marine turtles by generating high quality de novo blood transcriptome assemblies to characterize functional diversity and compare global transcriptional profiles between tissues, species, and foraging aggregations. Results We generated high quality blood transcriptome assemblies for hawksbill ( Eretmochelys imbricata ) , loggerhead ( Caretta caretta ), green ( Chelonia mydas ), and leatherback ( Dermochelys coriacea ) turtles. The functional diversity in assembled blood transcriptomes was comparable to those from more traditionally sampled tissues. A total of 31.3% of orthogroups identified were present in all four species, representing a core set of conserved genes expressed in blood and shared across marine turtle species. We observed strong species-specific expression of these genes, as well as distinct transcriptomic profiles between green turtle foraging aggregations that inhabit areas of greater or lesser anthropogenic disturbance. Conclusions Obtaining global gene expression data through non-lethal, minimally invasive sampling can greatly expand the applications of RNA-sequencing in protected long-lived species such as marine turtles. The distinct differences in gene expression signatures between species and foraging aggregations provide insight into the functional genomics underlying the diversity in this ancient vertebrate lineage. The transcriptomic resources generated here can be used in further studies examining the evolutionary ecology and anthropogenic impacts on marine turtles.

BMC Genomics

Biological nitrogen fixation: rates, patterns and ecological controls in terrestrial ecosystems

New techniques have identified a wide range of organisms with the capacity to carry out biological nitrogen fixation (BNF)—greatly expanding our appreciation of the diversity and ubiquity of N fixers—but our understanding of the rates and controls of BNF at ecosystem and global scales has not advanced at the same pace. Nevertheless, determining rates and controls of BNF is crucial to placing anthropogenic changes to the N cycle in context, and to understanding, predicting and managing many aspects of global environmental change. Here, we estimate terrestrial BNF for a pre-industrial world by combining information on N fluxes with 15 N relative abundance data for terrestrial ecosystems. Our estimate is that pre-industrial N fixation was 58 (range of 40–100) Tg N fixed yr −1 ; adding conservative assumptions for geological N reduces our best estimate to 44 Tg N yr −1 . This approach yields substantially lower estimates than most recent calculations; it suggests that the magnitude of human alternation of the N cycle is substantially larger than has been assumed.

Philosophical Transactions of the Royal Society B:

The extent of buildings in wildland vegetation of the conterminous U.S. and the potential for conservation in and near National Forest private inholdings

Development in natural areas is a leading threat to biodiversity. Global conservationists have called for the expansion of protected areas to preserve wildlands that are free from buildings, and in the U.S., the ‘America the Beautiful’ initiative aims to protect 30% of land and water areas by 2030 (known as the ‘30x30’ target). Here, we determined opportunities and limitations for conservation in the conterminous U.S. by assessing the extent of buildings in wildland vegetation. We focused specifically on National Forest lands, as these contain numerous private inholdings where development may occur. Using a newly available building footprint dataset, we determined 1) whether buildings were present and 2) numbers of buildings within three distances of wildland vegetation (100, 250, and 500 m), representing varying magnitudes of ecological impact. Our findings revealed that 29% of wildland vegetation nationwide was within 500 m of a building, 15% was within 250 m, and 5% was within 100 m. National Forest lands were less affected by building disturbance, but a substantial proportion (12%) of wildland vegetation area was within 500 m of a building. Of National Forest lands that were within 500 m of an inholding, 76% was not yet in proximity to a building; consequently, ∼10% of National Forest lands (143,474 km 2 ) are susceptible to impacts from future development on inholdings. We conclude that National Forest inholdings are therefore important opportunity areas for 30x30 conservation goals. Our assessments can inform where conservation efforts can limit impacts from present and future development on biodiversity.

Landscape and Urban Planning

Unbiased survival estimates and evidence for skipped breeding opportunities in females

1.  Estimates of demographic parameters for females, in many organisms, are sparse. This is particularly worrisome as more and more species are faced with high extinction probabilities and conservation increasingly depends on actions dictated by complex predictive models that require accurate estimates of demographic parameters for each sex and species. 2.  This study assesses demographic parameters, specifically temporary emigration and survival, for females, a class that has been difficult to investigate historically because of lack of data. Amphibians provide a particularly good example because there is global concern about amphibian decline; yet most demographic parameter estimates are based on data from males, which we show can lead to erroneous conclusions. 3.  We use 10 years of capture–recapture data from boreal toads ( Bufo boreas ) and the multi-state open robust design model to provide evidence for the occurrence of skipped breeding opportunities (i.e. temporary emigration) in females. This is the first time that the open robust design model has been applied to an analysis of an amphibian population that we are aware of. 4.  We determined that the transition from breeder to non-breeder is obligate and the probability of a non-breeder remaining a non-breeder is 64%; thus, temporary emigration is first-order Markovian in nature, where breeding probability is dependent on the previous year’s activity, i.e. if a female did not breed in year one, there is a 36% chance that she will breed in year two. With temporary emigration accounted for, we estimated between-year female survival at 87%. 5.  Establishing the occurrence of temporary emigration not only reduces bias in estimates of survival probabilities but also provides information about expected breeding attempts by females, a critical element in understanding the ecology of an organism and the impacts of outside stressors and conservation actions.

Methods in Ecology and Evolution

Eradication of peste des petits ruminants and the wildlife-livestock interface

Growing evidence suggests that multiple wildlife species can be infected with peste des petits ruminants virus (PPRV), with important consequences for the potential maintenance of PPRV in communities of susceptible hosts, and the threat that PPRV may pose to the conservation of wildlife populations and resilience of ecosystems. Significant knowledge gaps in the epidemiology of PPRV across the ruminant community (wildlife and domestic), and the understanding of infection in wildlife and other atypical host species groups (e.g., camelidae, suidae, and bovinae) hinder our ability to apply necessary integrated disease control and management interventions at the wildlife-livestock interface. Similarly, knowledge gaps limit the inclusion of wildlife in the FAO/OIE Global Strategy for the Control and Eradication of PPR, and the framework of activities in the PPR Global Eradication Programme that lays the foundation for eradicating PPR through national and regional efforts. This article reports on the first international meeting on, “Controlling PPR at the livestock-wildlife interface,” held in Rome, Italy, March 27–29, 2019. A large group representing national and international institutions discussed recent advances in our understanding of PPRV in wildlife, identified knowledge gaps and research priorities, and formulated recommendations. The need for a better understanding of PPRV epidemiology at the wildlife-livestock interface to support the integration of wildlife into PPR eradication efforts was highlighted by meeting participants along with the reminder that PPR eradication and wildlife conservation need not be viewed as competing priorities, but instead constitute two requisites of healthy socio-ecological systems.

Frontiers in Veterinary Science

Landscape transcriptomics as a tool for addressing global change effects across diverse species

Landscape transcriptomics is an emerging field studying how genome-wide expression patterns reflect dynamic landscape-scale environmental drivers, including habitat, weather, climate, and contaminants, and the subsequent effects on organismal function. This field is benefitting from advancing and increasingly accessible molecular technologies, which in turn are allowing the necessary characterization of transcriptomes from wild individuals distributed across natural landscapes. This research is especially important given the rapid pace of anthropogenic environmental change and potential impacts that span levels of biological organization. We discuss three major themes in landscape transcriptomic research: connecting transcriptome variation across landscapes to environmental variation, generating and testing hypotheses about the mechanisms and evolution of transcriptomic responses to the environment, and applying this knowledge to species conservation and management. We discuss challenges associated with this approach and suggest potential solutions. We conclude that landscape transcriptomics has great promise for addressing fundamental questions in organismal biology, ecology, and evolution, while providing tools needed for conservation and management of species.

Molecular Ecology Resources

Amphibians

Amphibians are ecologically important in most freshwater and terrestrial habitats in the United States: they can be numerous, function as both predators and prey, and constitute great biomass. Amphibians have certain physiological (e.g., permeable skin) and ecological (e.g., complex life cycle) traits that could justify their use as bioindicators of environmental health. For example, local declines in adult amphibians may indicate losses of nearby wetlands. The aquatic breeding habits of many terrestrial species result in direct exposure of egg, larval, and adult stages to toxic pesticides, herbicides, acidification, and other human-induced stresses in both aquatic and terrestrial habitats. Reported declines of amphibian populations globally have drawn considerable attention (Bury et al. 1980; Bishop and Petit 1992; Richards et al. 1993; Blaustein 1994; Pechmann and Wilbur 1994). Approximately 230 species of amphibians, including about 140 salamanders and 90 anurans (frogs and toads) occur in the continental United States. Because of their functional importance in most ecosystems, declines of amphibians are of considerable conservation interest. If these declines are real, the number of listed or candidate species at federal, state, and local levels could increase significantly. Unfortunately, because much of the existing information on status and trends of amphibians is anecdotal, coordinated monitoring programs are greatly needed.

Book chapter

Priorities for translating goodwill between movement ecologists and conservation practitioners into effective collaboration

Addressing ongoing biodiversity loss requires collaboration between conservation scientists and practitioners. However, such collaboration has proved challenging. Despite the potential importance of tracking animal movements for conservation, reviews of the tracking literature have identified a gap between the academic discipline of movement ecology and its application to biodiversity conservation. Through structured conversations with movement ecologists and conservation practitioners, we aimed to understand whether the identified gap is also perceived in practice, and if so, what factors hamper collaboration and how these factors can be remediated. We found that both groups are motivated and willing to collaborate. However, because their motivations differ, there is potential for misunderstandings and miscommunications. In addition, external factors such as funder requirements, academic metrics, and journal scopes may limit the applicability of scientific results in a conservation setting. Potential solutions we identified included improved communication and better presentation of results, acknowledging each other's motivations and desired outputs, and adjustment of funder priorities. Addressing gaps between science and implementation can enhance collaboration and support conservation action to address the global biodiversity crisis more effectively.

Conservation Science and Practice

Stress gradients structure spatial variability in coastal tidal marsh plant composition and diversity in a major Pacific coast estuary

Understanding the drivers of variability in plant diversity from local to landscape spatial scales is a challenge in ecological systems. Environmental gradients exist at several spatial scales and can be nested hierarchically, influencing patterns of plant diversity in complex ways. As plant community dynamics influence ecosystem function, understanding the drivers of plant community variability across space is paramount for predicting potential shifts in ecosystem function from global change. Determining the scales at which stress gradients influence vegetation composition is crucial to inform management and restoration of tidal marshes for specific functions. Here, we analyzed vegetation community composition in 51 tidal marshes from the San Francisco Bay Estuary, California, USA. We used model-based compositional analysis and rank abundance curves to quantify environmental (elevation/tidal frame position, distance to channel, and channel salinity) and species trait (species form, wetland indicator status, and native status) influences on plant community variability at the marsh site and estuary scales. While environmental impacts on plant diversity varied by species and their relationships to each other, overall impacts increased in strength from marsh to estuary scales. Relative species abundance was important in structuring these tidal marsh communities even with the limited species pools dominated by a few species. Rank abundance curves revealed different community structures by region with higher species evenness at plots higher in the tidal frame and adjacent to freshwater channels. By identifying interactions (species–species, species–environment, and environment–trait) at multiple scales (local, landscape), we begin to understand how variability measurements could be interpreted for conservation and land management decisions.

California

A structured decision-making framework for managing cyanobacterial harmful algal blooms in New York State parks

Cyanobacteria are increasingly a global water-quality concern because of the potential for these organisms to develop into potentially harmful blooms that affect ecological, economic, and public health. Cyanobacterial harmful algal blooms (CyanoHABs) can lead to a decrease in water quality and affect many of the recreational and ecological benefits of parks that include lakes. The New York State Office of Parks, Recreation and Historic Preservation (OPRHP) is a State agency within the New York State Executive Department charged with the operation of State parks and historic sites. Many New York State parks include lakes or other freshwater bodies, which can be susceptible to CyanoHABs. The OPRHP faces difficult decisions regarding prevention of and response to CyanoHABs. The U.S. Geological Survey partnered with the OPRHP and the New York State Department of Environmental Conservation to develop a structured decision-making template for managing CyanoHABs in OPRHP parks. Two parks, Moreau Lake State Park and Rockland Lake State Park, served as case studies to motivate and test the template. This report describes how the principles of structured decision making can be used to navigate the challenges associated with managing CyanoHABs in OPRHP parks. Management objectives and strategies for CyanoHABs in parks are described, strategies to evaluate consequences and manage tradeoffs are discussed, and potential challenges to the implementation of preferred alternatives are considered. General guidance is provided so the OPRHP can undertake the structured decision-making process for CyanoHABs in any of its parks. In addition, this report represents the first effort to create a strategy for applying decision analysis tools to the complex natural resource challenge of CyanoHAB mitigation and management. The case studies and template are intended to serve as an example that natural resource managers faced with CyanoHABs challenges can use to inform their decision-making processes.

New York

Demographic consequences of conservation reserve program grasslands for lesser prairie‐chickens

Knowledge of landscape and regional circumstances where conservation programs are successful on working lands in agricultural production are needed. Converting marginal croplands to grasslands using conservation programs such as the United States Department of Agriculture Conservation Reserve Program (CRP) should be beneficial for many grassland‐obligate wildlife species; however, addition of CRP grasslands may result in different population effects based on regional climate, characteristics of the surrounding landscape, or species planted or established. Within landscapes occupied by lesser prairie‐chickens (Tympanuchus pallidicinctus), CRP may provide habitat only for specific life stages and habitat selection for CRP may vary between wet and dry years. Among all study sites, we captured and fitted 280 female lesser prairie‐chickens with very high frequency (VHF)‐ and global positioning system (GPS) transmitters during the spring lekking seasons of 2013–2015 to monitor habitat selection for CRP in regions of varying climate. We also estimated vital rates and habitat selection for 148 individuals, using sites in northwest Kansas, USA. The greatest ecological services of CRP became apparent when examining habitat selection and densities. Nest densities were approximately 3 times greater in CRP grasslands than native working grasslands (i.e., grazed), demonstrating a population‐level benefit (CRP = 6.0 nests/10 km2 ± 1.29 [SE], native working grassland = 1.7 nests/10 km2 ± 0.62). However, CRP supporting high nest density did not provide brood habitat; 85% of females with broods surviving to 7 days moved their young to other cover types. Regression analyses indicated lesser prairie‐chickens were approximately 8 times more likely to use CRP when 5,000‐ha landscapes were 70% rather than 20% grassland, indicating variation in the level of ecological services provided by CRP was dependent upon composition of the larger landscape. Further, CRP grasslands were 1.7 times more likely to be used by lesser prairie‐chickens in regions receiving 40 cm compared to 70 cm of average annual precipitation and during years of greater drought intensity. Demographic and resource selection analyses revealed that establishing CRP grasslands in northwest Kansas can increase the amount nesting habitat in a region where it may have previously been limited, thereby providing refugia to sustain populations through periods of extreme drought. Nest survival, adult survival during breeding, and nonbreeding season survival did not vary between lesser prairie‐chickens that used and did not use CRP grasslands. The finite rate of population growth was also similar for birds using CRP and using only native working grasslands, suggesting that CRP provides habitat similar to that of native working grassland in this region. Overall, lesser prairie‐chickens may thrive in landscapes that are a mosaic of native working grassland, CRP grassland, with a minimal amount of cropland, particularly when nesting and brood habitat are in close proximity.

Journal of Wildlife Management