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A rapid, strong, and convergent genetic response to urban habitat fragmentation in four divergent and widespread vertebrates

Background: Urbanization is a major cause of habitat fragmentation worldwide. Ecological and conservation theory predicts many potential impacts of habitat fragmentation on natural populations, including genetic impacts. Habitat fragmentation by urbanization causes populations of animals and plants to be isolated in patches of suitable habitat that are surrounded by non-native vegetation or severely altered vegetation, asphalt, concrete, and human structures. This can lead to genetic divergence between patches and in turn to decreased genetic diversity within patches through genetic drift and inbreeding. Methodology/Principal Findings: We examined population genetic patterns using microsatellites in four common vertebrate species, three lizards and one bird, in highly fragmented urban southern California. Despite significant phylogenetic, ecological, and mobility differences between these species, all four showed similar and significant reductions in gene flow over relatively short geographic and temporal scales. For all four species, the greatest genetic divergence was found where development was oldest and most intensive. All four animals also showed significant reduction in gene flow associated with intervening roads and freeways, the degree of patch isolation, and the time since isolation. Conclusions/Significance: Despite wide acceptance of the idea in principle, evidence of significant population genetic changes associated with fragmentation at small spatial and temporal scales has been rare, even in smaller terrestrial vertebrates, and especially for birds. Given the striking pattern of similar and rapid effects across four common and widespread species, including a volant bird, intense urbanization may represent the most severe form of fragmentation, with minimal effective movement through the urban matrix.

California

Landscape change in the southern Piedmont: challenges, solutions, and uncertainty across scales

The southern Piedmont of the southeastern United States epitomizes the complex and seemingly intractable problems and hard decisions that result from uncontrolled urban and suburban sprawl. Here we consider three recurrent themes in complicated problems involving complex systems: (1) scale dependencies and cross-scale, often nonlinear relationships; (2) resilience, in particular the potential for complex systems to move to alternate stable states with decreased ecological and/or economic value; and (3) uncertainty in the ability to understand and predict outcomes, perhaps particularly those that occur as a result of human impacts. We consider these issues in the context of landscape-level decision making, using as an example water resources and lotic systems in the Piedmont region of the southeastern United States.

Conservation Ecology

Molecular genetics at the Fort Collins Science Center

The Fort Collins Science Center operates a molecular genetic and systematics research facility (FORT Molecular Ecology Laboratory) that uses molecular genetic tools to provide genetic information needed to inform natural resource management decisions. For many wildlife species, the data generated have become increasingly important in the development of their long-term management strategies, leading to a better understanding of species diversity, population dynamics and ecology, and future conservation and management needs. The Molecular Ecology Lab serves Federal research and resource management agencies by developing scientifically rigorous research programs using nuclear, mitochondrial and chloroplast DNA to help address many of today's conservation biology and natural resource management issues.

Fact Sheet

Assessing population-level consequences of anthropogenic stressors for terrestrial wildlife

Human activity influences wildlife. However, the ecological and conservation significances of these influences are difficult to predict and depend on their population‐level consequences. This difficulty arises partly because of information gaps, and partly because the data on stressors are usually collected in a count‐based manner (e.g., number of dead animals) that is difficult to translate into rate‐based estimates important to infer population‐level consequences (e.g., changes in mortality or population growth rates). However, ongoing methodological developments can provide information to make this transition. Here, we synthesize tools from multiple fields of study to propose an overarching, spatially explicit framework to assess population‐level consequences of anthropogenic stressors on terrestrial wildlife. A key component of this process is using ecological information from affected animals to upscale from count‐based field data on individuals to rate‐based demographic inference. The five steps to this framework are (1) framing the problem to identify species, populations, and assessment parameters; (2) field‐based measurement of the effect of the stressor on individuals; (3) characterizing the location and size of the populations of interest; (4) demographic modeling for those populations; and (5) assessing the significance of stressor‐induced changes in demographic rates. The tools required for each of these steps are well developed, and some have been used in conjunction with each other, but the entire group has not previously been unified together as we do in this framework. We detail these steps and then illustrate their application for two species affected by different anthropogenic stressors. In our examples, we use stable hydrogen isotope data to infer a catchment area describing the geographic origins of affected individuals, as the basis to estimate population size for that area. These examples reveal unexpectedly greater potential risks from stressors for the more common and widely distributed species. This work illustrates key strengths of the framework but also important areas for subsequent theoretical and technical development to make it still more broadly applicable.

Ecosphere

Satellite telemetry of marine megavertebrates: The coming of age of an experimental science

Wildlife telemetry research has expanded greatly in the last 2 decades, with the application of satellite tracking and archival logging technologies to study the ecology and conservation of marine mammals, birds, fishes, and turtles. Widespread and expanding use of satellite tracking to study movements and habitats of marine megavertebrates warrants a review of progress to date and a discussion of challenges facing this rapidly evolving research field. To this end, we reviewed the satellite telemetry literature of air-breathing marine taxa (i.e. birds, mammals, turtles) over the 20 yr time period from 1987 to 2006. This review yielded 92 studies with a wide taxonomic representation: 47 seabirds, 23 sea turtles, and 22 marine mammals. Here we critically evaluate these articles to assess progress in satellite tracking of marine megavertebrates in terms of (1) objectives and approach, (2) experimental design, and (3) reporting of results. The overall trends revealed increases in the duration and scope of tracking studies, yet improvements on experimental design and reporting are needed to facilitate comparisons across studies and species. While inherent ecological differences influence the focus and methods of taxon-specific studies, this review highlights specific areas in need of improvement and provides general suggestions for future tracking studies of marine megavertebrates.

Endangered Species Research

Maintenance and dissemination of avian-origin influenza A virus within the northern Atlantic Flyway of North America

Wild waterbirds, the natural reservoirs for avian influenza viruses, undergo migratory movements each year, connecting breeding and wintering grounds within broad corridors known as flyways. In a continental or global view, the study of virus movements within and across flyways is important to understanding virus diversity, evolution, and movement. From 2015 to 2017, we sampled waterfowl from breeding (Maine) and wintering (Maryland) areas within the Atlantic Flyway (AF) along the east coast of North America to investigate the spatio-temporal trends in persistence and spread of influenza A viruses (IAV). We isolated 109 IAVs from 1,821 cloacal / oropharyngeal samples targeting mallards (Anas platyrhynchos) and American black ducks (Anas rubripes) , two species having ecological and conservation importance in the flyway that are also host reservoirs of IAV. Isolates with >99% nucleotide similarity at all gene segments were found between eight pairs of birds in the northern site across years, indicating some degree of stability among genome constellations and the possibility of environmental persistence. No movement of whole genome constellations were identified between the two parts of the flyway, however, virus gene flow between the northern and southern study locations was evident. Examination of banding records indicate direct migratory waterfowl movements between the two locations within an annual season, providing a mechanism for the inferred viral gene flow. Bayesian phylogenetic analyses provided evidence for virus dissemination from other North American wild birds to AF dabbling ducks (Anatinae), shorebirds (Charidriformes), and poultry (Galliformes). Evidence was found for virus dissemination from shorebirds to gulls (Laridae), and dabbling ducks to shorebirds and poultry. The findings from this study contribute to the understanding of IAV ecology in waterfowl within the AF.

Chesapeake Bay

Integrating Sr isotopes, microchemistry, and genetics to reconstruct Salmonidae species and life history

Recent approaches to fisheries research emphasize the importance of the coproduction of knowledge in building resilient and culturally mindful fisheries management frameworks. Despite widespread recognition of the need for Indigenous knowledge and historical reference points as baseline data, archaeological data are rarely included in conservation biology research designs. Here we propose a novel multiproxy method to learn from former fisheries stewards by generating archaeological data on past salmonid population parameters. We used a newly developed, high throughput qPCR (HT-qPCR) chip, originally designed for environmental DNA (eDNA), for species identification of archaeological salmonid vertebrae. We combine this with the laser ablation split-stream (LASS) approach to identify ocean-migration versus freshwater residency. We test this multidisciplinary approach using both contemporary and archaeological salmonid samples and new radiocarbon dates from the Tronsdal Site on the Skagit River, Washington State, USA. This is a useful approach for extracting information about Salmonidae species and life history diversity from archaeological remains to reconstruct historic baselines for several population parameters in anadromous species with long periods of freshwater residency. The approach outlined in this paper may be particularly useful for research investigating past fisheries dynamics, offering hundreds to thousands of years of temporal depth for modern fisheries management, harvest policies, restoration ecology, and conservation biology.

Idaho, Oregon, Washington

Not so normal normals: Species distribution model results are sensitive to choice of climate normals and model type

Species distribution models have many applications in conservation and ecology, and climate data are frequently a key driver of these models. Often, correlative modeling approaches are developed with readily available climate data; however, the impacts of the choice of climate normals is rarely considered. Here, we produced species distribution models for five disparate species using four different modeling algorithms and compared results between two different, but overlapping, climate normals time periods. Although the correlation structure among climate predictors did not change between the time periods, model results were sensitive to both baseline climate period and model method, even with model parameters specifically tuned to a species. Each species and each model type had at least one difference in variable retention or relative ranking with the change in climate time period. Pairwise comparisons of spatial predictions were also different, ranging from a low of 1.6% for climate period differences to a high of 25% for algorithm differences. While uncertainty from model algorithm selection is recognized as an important source of uncertainty, the impact of climate period is not commonly assessed. These uncertainties may affect conservation decisions, especially when projecting to future climates, and should be evaluated during model development.

Climate

Mapping perceived social values to support a respondent-defined restoration economy: Case study in southeastern Arizona, USA

Investment in conservation and ecological restoration depends on various socioeconomic factors and the social license for these activities. Our study demonstrates a method for targeting management of ecosystem services based on social values, identified by respondents through a collection of social survey data. We applied the Social Values for Ecosystem Services (SolVES) geographic information systems (GIS)-based tool in the Sonoita Creek watershed, Arizona, to map social values across the watershed. The survey focused on how respondents engage with the landscape, including through their ranking of 12 social values (eg, recreational, economic, or aesthetic value) and their placement of points on a map to identify their associations with the landscape. Additional information was elicited regarding how respondents engaged with water and various land uses, as well as their familiarity with restoration terminology. Results show how respondents perceive benefits from the natural environment. Specifically, maps of social values on the landscape show high social value along streamlines. Life-sustaining services, biological diversity, and aesthetics were the respondents’ highest rated social values. Land surrounding National Forest and private lands had lower values than conservation-based and state-owned areas, which we associate with landscape features. Results can inform watershed management by allowing managers to consider social values when prioritizing restoration or conservation investments.

Arizona

A mechanistic understanding of ecological responses to land-use change in headwater streams

Anthropogenic activities, such as oil and natural gas development (ONGD), have significantly altered the landscape. It is often challenging to identify the mechanistic processes underlying ecological responses to land-use change (LUC). In aquatic ecosystems, alterations to habitat and food availability and water quality associated with increased LUC are key mechanistic pathways that deserve management consideration. We used structural equation modeling to evaluate how LUC associated with ONGD could influence macroinvertebrate and fish across 40 sites in six headwater streams in the Wyoming Range of the Upper Green River Basin, Wyoming. The most important mechanistic pathway varied, but responses were frequently driven by a direct effect of LUC or related to changes in food availability and water quality. Habitat complexity was the least important mechanistic pathway in our models. Our results also highlight that responses may reflect an organism's degree of habitat or resource specialization and/or sensitivity to changes in water quality. Habitat pathways were more important for habitat specialists (e.g., Mottled Sculpin, Cottus bairdii ), food pathways were more important for food specialists (e.g., Colorado River Cutthroat Trout, Oncorhynchus clarki pleuriticus ; Mountain Sucker, Catostomus platyrhynchus ), and sensitivity to increased salinity was important for intolerant species (e.g., O. clarki , C. bairdii , and predatory macroinvertebrates). Continued identification of the specific mechanisms underlying species’ responses to increased LUC will aid in the conservation of ecologically and economically important species.

Wyoming

[Book Review] Biology of marine birds

A text devoted to the biology and ecology of marine birds has not been published in the last 15 years. Although a number of more taxa-specific texts have been produced during that period, there has not been a single publication that attempted to review our knowledge of all the major seabird orders since the works of Nelson (1979), Croxall (1987), and Furness and Monaghan (1987). Following the publication of those works, a large and impressive body of literature has been produced. Given the rapid expansion of the field in the last two decades, the time was ripe for production of an extensive compendium on the biology, ecology, and conservation of the world's seabirds. E. A. Schreiber and J. Burger are editors of this CRC publication, Biology of Marine Birds . The book consists of 19 chapters that vary in length from 15 to 51 pages. There are also two extensive appendices: (1) a list of seabird species (restricted to the orders Sphenisciformes, Procellariiformes, Pelecaniformes, and Charadriiformes, the latter limited to Stercorariidae, Laridae, Rhynchopidae, and Alcidae) and their IUCN status, and (2) a very useful table of species-specific life-history traits. The 19 chapters were prepared by 26 authors, among them some of the most respected and published seabird scientists in the world. A brief preface introduces the book, its objective (to provide an examination and summary of the research on seabirds), its audience (researchers, conservationists, managers, and policy-makers), and the taxa covered. The editors coauthored the introductory chapter, Seabirds in the Marine Environment. The authors describe distinctive characteristics of seabird life-histories in comparison to other taxa, hypotheses for why those lifestyles evolved and the potential role of energy limitation in the evolution of seabird life-histories. Along with a discussion of other common seabird traits, such as a propensity for colonial breeding, the authors also suggest directions for future research in seabird ecology.

The Auk

Diel predator activity drives a dynamic landscape of fear

A “landscape of fear” (LOF) is a map that describes continuous spatial variation in an animal's perception of predation risk. The relief on this map reflects, for example, places that an animal avoids to minimize risk. Although the LOF concept is a potentially unifying theme in ecology that is often invoked to explain the ecological and conservation significance of fear, little is known about the daily dynamics of an LOF. Despite theory and data to the contrary, investigators often assume, implicitly or explicitly, that an LOF is a static consequence of a predator's mere presence within an ecosystem. We tested the prediction that an LOF in a large‐scale, free‐living system is a highly dynamic map with “peaks” and “valleys” that alternate across the diel (24‐h) cycle in response to daily lulls in predator activity. We did so with extensive data from the case study of Yellowstone elk ( Cervus elaphus ) and wolves ( Canis lupus ) that was the original basis for the LOF concept. We quantified the elk LOF, defined here as spatial allocation of time away from risky places and times, across nearly 1,000‐km 2 of northern Yellowstone National Park and found that it fluctuated with the crepuscular activity pattern of wolves, enabling elk to use risky places during wolf downtimes. This may help explain evidence that wolf predation risk has no effect on elk stress levels, body condition, pregnancy, or herbivory. The ability of free‐living animals to adaptively allocate habitat use across periods of high and low predator activity within the diel cycle is an underappreciated aspect of animal behavior that helps explain why strong antipredator responses may trigger weak ecological effects, and why an LOF may have less conceptual and practical importance than direct killing.

Yellowstone National Park

Long-term apparent survival of a cold-stunned subpopulation of juveniles green turtles

Understanding the effects of extreme weather on animal populations is fundamental to ecological and conservation sciences and species management. Climate change has resulted in both warm and cold temperature extremes, including an increased frequency of severe cold snaps at middle latitudes in North America. These unusually cold air masses cause rapid declines in nearshore ocean temperatures in coastal areas, with detrimental effects on marine organisms. Acute cold-stun events (hereafter cold stuns) occur when hundreds to thousands of resident juvenile sea turtles fail to escape shallow water during cold snaps. Human intervention through rescue and recovery largely mitigates direct juvenile sea turtle mortality, but delayed effects of cold stuns on rescued individuals are not well understood. Our objective was to examine long-term juvenile green turtle ( Chelonia mydas ) survival across four cold stuns of varying severity in St. Joseph Bay, Florida, between 2010 and 2018. We used the classic Cormack–Jolly–Seber model in a hierarchical Bayesian framework to estimate apparent survival (i.e., emigration and mortality) of rescued turtles at different time intervals. Our results indicated about half of a cohort rescued during a severe cold stun in January 2010 likely remained in the population 1 year later, with 10%–20% remaining 4 years later, and as few as 5% by 2018. The results also suggested higher apparent survival for cohorts rescued during two subsequent milder cold stuns. Emigration was a more plausible ecological explanation for low apparent survival than delayed mortality. Potential ecological mechanisms underlying emigration include a reduction in food availability and a behavioral response to either the severe weather event or handling during rescue (or both). However, the typical annual turnover of juvenile green turtles, though assumed low, is not well known in St. Joseph Bay. Thus, our apparent survival estimates may be reflective of higher-than-expected emigration in the broader population. Our study provides important baseline information about long-term juvenile sea turtle survival after cold stuns in temperate regions. We also highlight the importance of strategic monitoring between cold stuns to examine additional ecological questions.

Florida

Data management challenges in species distribution modeling

An important component in the fields of ecology and conservation biology is understanding the environmental conditions and geographic areas that are suitable for a given species to inhabit. A common tool in determining such areas is species distribution modeling which uses computer algorithms to determine the spatial distribution of organisms. Most commonly the correlative relationships between the organism and environmental variables are the primary consideration. The data requirements for this type of modeling consist of known presence and possibly absence locations of the species as well as the values of environmental or climatic covariates thought to define the species habitat suitability at these locations. These covariate data are generally extracted from remotely sensed imagery, interpolated/gridded historical climate data, or downscaled climate model output. Traditionally, ecologists and biologists have constructed species distribution models using workflows and data that reside primarily on their local workstations or networks. This workflow is becoming challenging as scientists increasingly try to use these modeling techniques to inform management decisions under different climate change scenarios. This challenge stems from the fact that remote sensing products, gridded historical climate, and downscaled climate models are not only increasing in spatial and temporal resolution but proliferating as well. Any rigorous assessment of uncertainty requires a computationally intensive sensitivity analysis accounting for various sources of uncertainty. The scientists fitting these models generally do not have the background in computer science required to take advantage of recent advances in web-service based data acquisition, remote high-powered data processing, or scientific workflow systems. Ecologists in the field of modeling are in need of a tractable platform that abstracts the inherent computational complexity required to incorporate the burgeoning field of coupled climate and ecological response modeling. In this paper we describe the computational challenges in species distribution modeling and solutions using scientific workflow systems. We focus on the Software for Assisted Species Modeling (SAHM) a package within VisTrails, an open-source scientific workflow system.

Bulletin of the Technical Committee on Data Engine

Critical considerations for the application of environmental DNA methods to detect aquatic species

Species detection using environmental DNA (eDNA) has tremendous potential for contributing to the understanding of the ecology and conservation of aquatic species. Detecting species using eDNA methods, rather than directly sampling the organisms, can reduce impacts on sensitive species and increase the power of field surveys for rare and elusive species. The sensitivity of eDNA methods, however, requires a heightened awareness and attention to quality assurance and quality control protocols. Additionally, the interpretation of eDNA data demands careful consideration of multiple factors. As eDNA methods have grown in application, diverse approaches have been implemented to address these issues. With interest in eDNA continuing to expand, supportive guidelines for undertaking eDNA studies are greatly needed. Environmental DNA researchers from around the world have collaborated to produce this set of guidelines and considerations for implementing eDNA methods to detect aquatic macroorganisms. Critical considerations for study design include preventing contamination in the field and the laboratory, choosing appropriate sample analysis methods, validating assays, testing for sample inhibition and following minimum reporting guidelines. Critical considerations for inference include temporal and spatial processes, limits of correlation of eDNA with abundance, uncertainty of positive and negative results, and potential sources of allochthonous DNA. We present a synthesis of knowledge at this stage for application of this new and powerful detection method.

Methods in Ecology and Evolution

Physiological consequences of consuming low-energy foods: Herbivory coincides with a stress response in Yellowstone bears.

Meat, fruit, seeds and other high-energy bear foods are often highly localized and briefly available and understanding which factors influence bear consumption of these foods is a common focus of bear conservation and ecology. However, the most common bear foods, graminoids and forbs, are more widespread but of lower quality. We poorly understand how herbage consumption impacts bear physiology, such as endocrine system function that regulates homeostasis and stress responses. Here, we described bear diets with a novel approach, measuring the concentration of chlorophyll in bear scats (faecal chlorophyll) to index the proportion of the recent diet that was composed of leaves from graminoids and forbs. We measured faecal chlorophyll and faecal cortisol in 351 grizzly ( Ursus arctos , n = 255) and black bear ( Ursus americanus , n = 96) scats from Yellowstone National Park in 2008–2009. We compared models of faecal chlorophyll and faecal cortisol concentrations considering the effects of spatial, dietary, scat and bear-specific factors including species. Faecal chlorophyll levels were the strongest predictor of faecal cortisol in a manner that suggested an endocrine response to a low-energy diet. Both compounds were highest during the spring and early summer months, overlapping the breeding season when higher energy foods were less available. Effects of scat composition, scat weathering, bear age, bear sex, species and other factors that have previously been shown to influence faecal cortisol in bears were not important unless faecal chlorophyll was excluded from models. The top models of faecal chlorophyll suggested grazing was primarily influenced by spatial attributes, with greater grazing closer to recreational trails, implying that elevated cortisol with grazing could be a response to anthropogenic activity. Our results confirm that higher stress hormone concentrations correspond with lower quality diets in bears, particularly grazing, and that faecal chlorophyll shows promise as a metric for studying grazing behaviour and its consequences.

Wyoming

Landscape characteristics influencing the genetic structure of greater sage-grouse within the stronghold of their range: a holistic modeling approach

Given the significance of animal dispersal to population dynamics and geographic variability, understanding how dispersal is impacted by landscape patterns has major ecological and conservation importance. Speaking to the importance of dispersal, the use of linear mixed models to compare genetic differentiation with pairwise resistance derived from landscape resistance surfaces has presented new opportunities to disentangle the menagerie of factors behind effective dispersal across a given landscape. Here, we combine these approaches with novel resistance surface parameterization to determine how the distribution of high- and low-quality seasonal habitat and individual landscape components shape patterns of gene flow for the greater sage-grouse ( Centrocercus urophasianus ) across Wyoming. We found that pairwise resistance derived from the distribution of low-quality nesting and winter, but not summer, seasonal habitat had the strongest correlation with genetic differentiation. Although the patterns were not as strong as with habitat distribution, multivariate models with sagebrush cover and landscape ruggedness or forest cover and ruggedness similarly had a much stronger fit with genetic differentiation than an undifferentiated landscape. In most cases, landscape resistance surfaces transformed with 17.33-km-diameter moving windows were preferred, suggesting small-scale differences in habitat were unimportant at this large spatial extent. Despite the emergence of these overall patterns, there were differences in the selection of top models depending on the model selection criteria, suggesting research into the most appropriate criteria for landscape genetics is required. Overall, our results highlight the importance of differences in seasonal habitat preferences to patterns of gene flow and suggest the combination of habitat suitability modeling and linear mixed models with our resistance parameterization is a powerful approach to discerning the effects of landscape on gene flow.

Ecology and Evolution

Integrating growth and survival models for flexible estimation of size-dependent survival in a cryptic, endangered snake

Estimates of demographic rates for animal populations and individuals have many applications for ecological and conservation research. In many animals, survival is size-dependent, but estimating the form of the size–survival relationship presents challenges. For elusive species with low recapture rates, individuals’ size will be unknown at many points in time. Integrating growth and capture–mark–recapture models in a Bayesian framework empowers researchers to impute missing size data, with uncertainty, and include size as a covariate of survival, capture probability, and presence on-site. If there is no theoretical expectation for the shape of the size–survival relationship, spline functions can allow for fitting flexible, data-driven estimates. We use long-term capture–mark–recapture data from the endangered San Francisco gartersnake ( Thamnophis sirtalis tetrataenia ) to fit an integrated growth–survival model. Growth models showed that females reach longer asymptotic lengths than males and that the magnitude of sexual size dimorphism differed among populations. The capture probability and availability of San Francisco gartersnakes for capture increased with snout–vent length. The survival rate of female snakes exhibits a nonlinear relationship with snout–vent length (SVL), with survival flat between 300 mm and 550 mm SVL before decreasing for females between 550 mm and 700 mm SVL. For male snakes, survival decreased for adult males >550 mm SVL. The survival rates of the smallest and largest San Francisco gartersnakes were highly uncertain because recapture rates were very low for these sizes. By integrating growth and survival models and using penalized splines, we found support for size-dependent survival in San Francisco gartersnakes. Our results have applications for devising management activities for this endangered subspecies, and our methods could be applied broadly to the study of size-dependent demography among animals.

California