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A pragmatic approach for integrating molecular tools into biodiversity conservation

Molecular tools are increasingly applied for assessing and monitoring biodiversity and informing conservation action. While recent developments in genetic and genomic methods provide greater sensitivity in analysis and the capacity to address new questions, they are not equally available to all practitioners: There is considerable bias across institutions and countries in access to technologies, funding, and training. Consequently, in many cases, more accessible traditional genetic data (e.g., microsatellites) are still utilized for making conservation decisions. Conservation approaches need to be pragmatic by tackling clearly defined management questions and using the most appropriate methods available, while maximizing the use of limited resources. Here we present some key questions to consider when applying the molecular toolbox for accessible and actionable conservation management. Finally, we highlight a number of important steps to be addressed in a collaborative way, which can facilitate the broad integration of molecular data into conservation.

Conservation Science and Practice

Biodiversity: a new challenge

Resource managers at many state and federal agencies are in the middle of a fundamental change in the practice and objectives of conservation. Traditional management has been directed toward maintaining, usually for harvest purposes, populations of individual species such as ducks, deer, or salmon. Increasingly, however, resource managers are recognizing the critical important of conserving biological diversity, or biodiversity. In its simplest terms, biological diversity is the variety of life at all levels: it includes the array of plants and animals; the genetic differences among individuals; the communities, ecosystems, and landscapes in which they occur; and the variety of processes on which they depend. Conserving biological diversity poses dramatic new problems for comprehensive inventory and monitoring: what should be measured or monitored?

Book chapter

The interplay of species concepts, taxonomy, and conservation: lessons from the Hawaiian avifauna

The Hawaiian Islands, with their unique geological history and geographic position, provide an excellent natural laboratory in which to evaluate currently competing biological (BSC) and phylogenetic (PSC) concepts of the species. Although the BSC as historically applied in archipelagic situations is shown to be flawed in producing overlumped polytypic species, it nevertheless remains the preferable concept for most practical purposes. A review of the taxonomic history and species limits in Hawaiian birds under both concepts reveals that, when properly applied, the BSC yields a species total remarkably close to that produced under the PSC, contrary to what many proponents of the latter have supposed. We propose that the widespread adoption of the PSC for conservation purposes is potentially harmful. The PSC trivializes the species taxon and introduces new problems of deciding when a population becomes diagnosable, the possibility that species could appear and disappear in a reticulate fashion, and the likelihood that genetically diagnosable but phenotypically identical, and therefore not field identifiable, populations could be ranked as species. All of these problems negatively impact such things as constructing credible and politically defensible lists of endangered species, the prioritization of limited conservation resources, and the gathering of field data. We contend the BSC is arguably a more rational concept that better supports the activities of both scientific and nonprofessional observers. Biological species limits in oceanic archipelagoes worldwide need to be reevaluated using modern concepts and technologies before rational conservation decisions can be made.

Hawaii

Improving conservation outcomes with a new paradigm for understanding species’ fundamental and realized adaptive capacity

Worldwide, many species are responding to ongoing climate change with shifts in distribution, abundance, phenology, or behavior. Consequently, natural-resource managers face increasingly urgent conservation questions related to biodiversity loss, expansion of invasive species, and deteriorating ecosystem services. We argue that our ability to address these questions is hampered by the lack of explicit consideration of species’ adaptive capacity (AC). AC is the ability of a species or population to cope with climatic changes and is characterized by three fundamental components: phenotypic plasticity, dispersal ability, and genetic diversity. However, few studies simultaneously address all elements; often, AC is confused with sensitivity or omitted altogether from climate-change vulnerability assessments. Improved understanding, consistent definition, and comprehensive evaluations of AC are needed. Using classic ecological-niche theory as an analogy, we propose a new paradigm that considers fundamental and realized AC: the former reflects aspects inherent to species, whereas the latter denotes how extrinsic factors constrain AC to what is actually expressed or observed. Through this conceptualization, we identify ecological attributes contributing to AC, outline areas of research necessary to advance understanding of AC, and provide examples demonstrating how the inclusion of AC can better inform conservation and natural-resource management.

Conservation Letters

The potential influence of genome-wide adaptive divergence on conservation translocation outcome in an isolated greater sage-grouse population

Conservation translocations are an important conservation tool commonly employed to augment declining or reestablish extirpated populations. One goal of augmentation is to increase genetic diversity and reduce the risk of inbreeding depression (i.e., genetic rescue). However, introducing individuals from significantly diverged populations risks disrupting coadapted traits and reducing local fitness (i.e., outbreeding depression). Genetic data are increasingly more accessible for wildlife species and can provide unique insight regarding the presence and retention of introduced genetic variation from augmentation as an indicator of effectiveness and adaptive similarity as an indicator of source and recipient population suitability. We used 2 genetic data sets to evaluate augmentation of isolated populations of greater sage-grouse ( Centrocercus urophasianus ) in the northwestern region of the species range (Washington, USA) and to retrospectively evaluate adaptive divergence among source and recipient populations. We developed 2 statistical models for microsatellite data to evaluate augmentation outcomes. We used one model to predict genetic diversity after augmentation and compared these predictions with observations of genetic change. We used the second model to quantify the amount of observed reproduction attributed to transplants (proof of population integration). We also characterized genome-wide adaptive divergence among source and recipient populations. Observed genetic diversity ( H O = 0.65) was higher in the recipient population than predicted had no augmentation occurred ( H O = 0.58) but less than what was predicted by our model ( H O = 0.75). The amount of shared genetic variation between the 2 geographically isolated resident populations increased, which is evidence of periodic gene flow previously assumed to be rare. Among candidate adaptive genes associated with elevated fixation index ( F ST ) (143 genes) or local environmental variables (97 and 157 genes for each genotype–environment association method, respectively), we found clusters of genes with related functions that may influence the ability of transplants to use local resources and navigate unfamiliar environments and their reproductive potential, all possible reasons for low genetic retention from augmentation.

Conservation Biology

The LTAR Grazing Land Common Experiment at the Jornada Experimental Range: Old genetics, new precision technologies, and adaptive value chains

Rangelands and the supply chains connected to them are central to the agrifood systems of the Southwestern United States. Local ranchers are simultaneously arid lands managers, herd managers, and marketing managers. To stay in business, they must constantly adapt to unpredictable forage resources and markets while conserving soils and vegetation resources for the long term. As climate warming and drying exacerbate the complexity and difficulty of day-to-day production, producers and policy-makers are seeking alternatives to “business as usual”. To meet this need, the LTAR-Jornada team has developed a package of strategies to help producers adapt to the local and inter-regional challenges. The package includes heritage cattle, precision ranching systems, and adaptive value chains. Five ranches across the Southwest have adopted different combinations of the strategies and are partnering to measure their benefits and drawbacks in real-world conditions. Opportunities for controlled experimentation differ among the ranches, so we use LTAR’s indicator system to assess and compare results. Even as we invest in co-producing knowledge about these three strategies, we recognize that progressive aridification and urbanization of Southwestern rangelands create challenges for which a single “silver bullet” agricultural innovation is unlikely to provide durable solutions. We are learning from our customers and stakeholders about ways to adjust the development of new options.

New Mexico

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

Combining individual and close-kin mark–recapture to design an effective wildlife population survey

Close-kin mark–recapture (CKMR) is a promising approach for assessing population size of species that have been difficult to survey using more traditional methods. Here, we combine individual and close-kin mark–recapture in a single modeling framework (ICKMR) and provide an example of study design using this approach for Pacific walrus ( Odobenus rosmarus divergens ). We develop the ICKMR model and test it using simulated datasets, then use properties of the pseudo-likelihood to investigate the expected precision in estimates of abundance with different proposed survey designs. Our motivating example, the Pacific walrus, is an ice-associated marine mammal found in the Bering and Chukchi seas, where it is an important resource for Indigenous peoples. Pacific walrus abundance declined in the late 20th century, and it is currently a species of conservation concern due to potential impacts of climate change, particularly the loss of sea ice. To reduce uncertainty in population size estimates, researchers undertook a genetic mark–recapture sampling campaign from 2013 to 2017 and collected tissue samples from over 8000 individuals. Another campaign of a similar scale is ongoing (2023–2028). While sample collection was designed for individual mark–recapture, advances in CKMR methods and associated molecular techniques mean that these samples could also be suitable for CKMR. The advantages of CKMR over mark–recapture include an increased effective sample size (because each individual tags itself and its parents, siblings, and offspring) and additional insights into demographic quantities of interest. To make best use of genetic samples, we combine individual mark–recapture (IMR) with CKMR (ICKMR) and investigate whether different sampling strategies can increase precision in estimates of abundance. Our modeling approach includes special considerations for walrus life history, including a multi-year inter-birth interval. We found that expected coefficients of variation (CVs) of the ICKMR estimates of abundance, adult female survival, juvenile female survival, and proportion of breeding females are lower than those expected from IMR alone, and with ICKMR, fewer years of sampling can be conducted to obtain sufficient precision in estimates of abundance. This work demonstrates the utility of ICKMR and could be applicable across a variety of taxa.

Ecology

Forage and habitat for pollinators in the northern Great Plains—Implications for U.S. Department of Agriculture conservation programs

Managed and wild pollinators are critical components of agricultural and natural systems. Despite the well-known value of insect pollinators to U.S. agriculture, Apis mellifera (Linnaeus, 1758; honey bees) and wild bees currently face numerous stressors that have resulted in declining health. These declines have engendered support for pollinator conservation efforts across all levels of government, private businesses, and nongovernmental organizations. In 2014, the U.S. Department of Agriculture (USDA) and the U.S. Geological Survey initiated an interagency agreement to evaluate honey bee forage across multiple States in the northern Great Plains and upper Midwest. The long-term goal of this study was to provide an empirical evaluation of floral resources used by honey bees, and the relative contribution of multiple land covers and USDA conservation programs to bee health and productivity. Our multi-State analysis of land-use change from 2006 to 2016 revealed loss of grassland and increases in corn and soybean area in North and South Dakota, representing a significant loss of bee-friendly land covers in areas that support the highest density of summer bee yards in the entire United States. Our landscape models demonstrate the importance of the Conservation Reserve Program in providing safe locations for beekeepers to keep honey bees during the summer and highlights how land use in the northern Great Plains has a lasting effect on the health of honey bee colonies during almond pollination the subsequent spring. Our multiseason, multi-State genetic analysis of honey bee-collected pollen revealed Melilotus spp., Asteraceae, Trifolium spp., Fabaceae, Sonchus arvensis , Symphyotrichum cordifolium , and Solidago spp. were the top taxa detected; Melilotus spp. represented 42 percent of all detected taxa. Symphyotrichum cordifolium , Solidago spp., and Grindelia spp. were the top native forbs detected in honey bee-collected pollen. We also conducted plant and bee surveys on private lands enrolled in the Conservation Reserve Program and Environmental Quality Incentives Program. In general, we found significant variability in floral resources and pollinator utilization across USDA programs and practices. On average, greater than 75 percent of honey bee flower observations on private lands enrolled in a USDA conservation program were on non-native forbs, whereas 33 percent of wild bee flower observations were on non-native forbs. Melilotus officinalis and Medicago sativa were the most visited by honey bees, wherease Medicago sativa and Helianthus maximiliani were the most visited by wild bees. Our analysis of nectar dearth periods in June and September for honey bees revealed that although Melilotus officinalis and Medicago sativa were highly visited, less common native forb species such as Ratibida columnifera , Agastache foeniculum , and Gaillardia aristata were preferred species. However, these preferred species were relatively rare on the landscape and are, therefore, unlikely to make up a sizable part of the honey bee diet. In addition to our empirical results, we also showcase how the U.S. Geological Survey Pollinator Library, a decision-support tool for natural resource managers, can be used to design cost-effective seeding mixes for pollinators. Collectively, the results of this research will assist USDA with maximizing the ecological impact and cost-effectiveness of their conservation programs on pollinators in the northern Great Plains.

Minnesota, North Dakota, South Dakota

Spatially explicit management of genetic diversity using ancestry probability surfaces

1. Ecological restoration and conservation efforts are increasing worldwide and the management of intraspecific genetic variation in plants and animals, an important component of biodiversity, is increasingly valued. As a result, tailorable, spatially explicit approaches to map genetic variation are needed to support decision-making and management frameworks related to the recovery of threatened and endangered species and the maintenance of genetic resources in species utilized by humans, such as for restoration or agricultural purposes. 2. Here, we describe and demonstrate a workflow to spatially interpolate patterns of genetic differentiation using novel functions in the R package POPMAPS ( Pop ulation M anagement using A ncestry P robability S urfaces). Our approach uses empirical genetic data to estimate ancestry coefficients across a user-defined landscape correlated with patterns of differentiation in the focal species. The resulting surface, which we term the ancestry probability surface, includes two components: hard population boundaries and estimations of uncertainty that represent confidence in population assignments (i.e., ancestry probabilities). 3. An ancestry probability surface developed for Hilaria jamesii , an important graminoid utilized in restoration across the western United States, demonstrates the functionality of POPMAPS . Genetic distances among empirical sites correlated better with least-cost distances across suitable habitat than with geographic distances, informing the surface over which the interpolation was conducted (i.e., a model indicating habitat suitability). A jackknifing procedure identified parameter values resulting in robust population assignments across the species’ range, which were utilized in downstream analyses to estimate ancestry coefficients from empirical data. Ancestry coefficients were translated into ancestry probabilities, which tended to be low for cells that were intermediate in distance between empirical sampling locations representing different populations or when influenced by empirical sampling locations with mixed genetic ancestry. 4. POPMAPS allows users to tailor parameter values and analytical approaches and thereby incorporate species-specific biological characteristics and desired levels of uncertainty into maps illustrating patterns of genetic differentiation. Ancestry probability surfaces may be used to guide management or investigate further ecological or evolutionary hypotheses. We discuss how maps produced by POPMAPS can inform multiple management challenges including species recovery planning and the utilization of commonly used species in restoration.

Methods in Ecology and Evolution

Linking resource selection to population performance spatially to identify species' habitat across broad scales: An example of greater sage-grouse in a distinct population segment

Management decisions often focus on the habitat selection of marked individuals without considering the contribution to demographic performance in selected habitats. Because habitat selection is not always adaptive, understanding the spatial relationship between habitat selection and demographic performance is critical to management decisions. Mapping both habitat selection and demographic performance for species of conservation concern can help guide population-scale conservation efforts. We demonstrate a quantitative approach to differentiate areas supporting selection and survival at large spatial extents. As a case study, we applied this approach to greater sage-grouse ( Centrocercus urophasianus ; hereafter, sage-grouse), an indicator species for sagebrush ecosystems. We evaluated both habitat selection and survival across multiple reproductive life stages (nesting, brood-rearing) in the Bi-State Distinct Population Segment, a genetically distinct and geographically isolated population of sage-grouse on the southwestern edge of the species' range. Our approach allowed us to identify both mismatches between selection and survival and trade-offs between reproductive life stages. These findings suggest resource demands vary across time, with predation risk being a dominant driver of habitat selection during nesting and early brood-rearing periods when chicks are smaller and flightless, whereas access to forage resources becomes more important during late brood rearing when resources become increasingly limited. Moving beyond identifying and managing habitat solely based on species occupancy or use by incorporating demographic measures allows managers to tailor actions to their specific goals; for example, protections of areas that support high selection and high survival and restoration actions focused on increasing survival in areas of high selection and low survival.

California, Nevada

Engaging stakeholders to develop a decision support model of conservation risk and management capacity to prioritize investments in Bull Trout recovery

Rarely are sufficient resources available to support the full suite of management actions to promote recovery of a species across their entire distribution. Decision support models are a tool that can inform natural resource management decisions with consideration of the perspectives from a variety of stakeholders who work across large geographic and jurisdictional extents. We offer an example of a decision support model that was developed by several Federal and State natural resource agencies to rank Bull Trout Salvelinus confluentus core areas for prioritizing conservation investment within Oregon, USA. We engaged State level decision makers to identify parameters believed to be influential in determining funding allocations for Bull Trout core areas. Parameters were linked in a model framework that was further refined with input from local Bull Trout experts with knowledge specific to the various core areas. The model produces a relative priority value that is a combination of the conservation risk to the species and the management capacity to address threats. A series of sensitivity analyses suggests that Bull Trout persistence and threat score are most influential in determining the relative priority of a core area, and life-history and genetic diversity are least influential. One of the more powerful products from this work is an interactive web-based application ( https://das.ecosphere.fws.gov/public/obts/ ) that anyone can use to explore how their beliefs in parameter values will affect the relative priority of Bull Trout core areas across Oregon. Our modeling effort is an example of engaging stakeholders with different roles in species recovery and across a large geographic area to create a clearer path forward in allocating limited resources for species recovery. This approach can be employed to address a number of natural resource management situations across species and habitats.

Oregon

Haploid gynogens facilitate disomic marker development in paleotetraploid sturgeons

Acipenseriformes (sturgeons and paddlefishes) are of substantial conservation concern, and development of genomic resources for these species is difficult due to past whole genome duplication. Development of disomic markers for polyploid organisms can be challenging due to difficulty in resolving alleles at a single locus from those among duplicated loci. In this study, we detail the development of disomic markers for the endangered pallid sturgeon ( Scaphirhynchus albus ) found in North America. One of the strategies for pallid sturgeon conservation is to stock U.S. rivers with offspring of pure pallid sturgeon, but introgression with the sympatric shovelnose sturgeon ( S. platorynchus ) threatens pallid sturgeon genetic integrity. Currently, 19 microsatellite loci are used to differentiate between both species and their hybrids, but the markers are insufficient to robustly identify backcrosses. We performed double digest restriction site-associated DNA sequencing (ddRADseq) on shovelnose sturgeon haploid gynogens to produce a reduced-representation genomic reference. Contiguous sequences that were heterozygous within a haploid individual were flagged as potentially encompassing multiple loci. Approximately 60 individuals of each species from two management units were sequenced, and reads were mapped to the haploid reference to identify single nucleotide polymorphisms (SNPs) at individual loci. The final data set contained 11,082 microhaplotyped loci which offer at least an order of magnitude greater resolution for species discrimination than the current panel of 19 microsatellites. These markers will be used to examine a larger sample of Scaphirhynchus individuals throughout their ranges to determine the extent and trajectory of hybridization.

Molecular Ecology Resources

Will an "island" population of voles be recolonized if eradicated? Insights from molecular genetic analyses

We performed genetic analyses of Microtus longicaudus populations within the Crook Point Unit of the Oregon Islands National Wildlife Refuge. A M. longicaudus population at Saddle Rock (located approx. 65 m off‐shore from the Crook Point mainland) is suspected to be partially responsible for declines of a Leach's storm‐petrel colony at this important nesting site. Using Amplified Fragment Length Polymorphism markers and mitochondrial DNA, we illustrate that Saddle Rock and Crook Point function as separate island and mainland populations despite their close proximity. In addition to genetic structure, we also observed reduced genetic diversity at Saddle Rock, suggesting that little individual movement occurs between populations. If local resource managers decide to perform an eradication at Saddle Rock, we conclude that immediate recolonization of the island by M. longicaudus would be unlikely. Because M. longicaudus is native to Oregon, we also consider the degree with which the differentiation of Saddle Rock signifies the presence of a unique entity that warrants conservation rather than eradication

Oregon

Minimizing extinction risk in the face of uncertainty: Developing conservation strategies for 2 rapidly declining forest bird species on Kaua‘i Island

Many species around the world are declining precipitously as a result of multiple threats and changing climate. Managers tasked with protecting species often face difficult decisions in regard to identifying which threats should be addressed, given limited resources and uncertainty in the success of any identified management action. On Kaua‘i Island, Hawai‘i, USA, forest bird species have experienced accelerated declines over the last 20 years, and 2 species, the ‘akikiki ( Oreomystis bairdi ) and ‘akeke‘e ( Loxops caeruleirostris ), are now at the brink of extinction. Both species face multiple threats, and managers face difficult decisions on whether to mitigate threats in the wild, establish a captive population as insurance against extinction, translocate birds to novel locations, or some combination of these actions. Each set of actions (alternatives) would require substantial resources with considerable uncertainty in success. In 2014, we brought together 14 experts representing biologists and managers familiar with the species and island to develop a conservation strategy under a structured decision making (SDM) framework, an approach for making complex decisions under uncertainty. The group's challenge was to identify a set of alternatives that reduces the risk of extinction, set the foundation for one or more genetically viable, reproducing, stable to increasing populations in 10 years, and promote conditions for long-term persistence in the wild. Multiple alternatives were evaluated, via expert judgement, in terms of the probability they would achieve the objectives concerning immediate extinction risk, near-term viability, and adequacy of habitat. Factors that might impede the success of each action were also evaluated. The process identified the establishment of a captive population and efforts to stabilize the existing wild population as the approach most likely to meet the objectives of preventing imminent extinction and ensuring long-term viability.

Hawaii

Development of microsatellite markers for three at risk tiger beetles Cicindela dorsalis dorsalis, C. d. media, and C. puritana

Objective Tiger beetles inhabiting sandy beaches and cliffs along the east coast of the United States are facing increasing habitat loss due to erosion, urbanization, and sea level rise. The northeastern beach tiger beetle Cicindela dorsalis dorsalis and Puritan tiger beetle Cicindela puritana are both listed as threatened under the Endangered Species Act of 1973, while the white beach tiger beetle Cicindela dorsalis media is not listed but has been declining. Extirpation of these beetles, in some cases from entire states, has isolated many populations reducing gene flow and elevating the risk for the loss of genetic variation. To facilitate investigations of population genetic structure, we developed suites of microsatellite loci for conservation genetic studies. Results Shotgun genomic sequencing of all species identified thousands of candidate microsatellite loci, among which 17 loci were optimized and verified to cross-amplify within C. d. media and C. d. dorsalis , and eight separate loci were optimized for C. puritana . Most loci conformed to Hardy–Weinberg equilibrium, showed no evidence of linkage disequilibrium or null alleles, and revealed population genetic characteristics informative for natural resource managers among the populations tested.

BMC Research Notes

Between hot rocks and dry places: The status of the Dixie Valley toad

In Dixie Valley, Nevada, an isolated population of toads has been the subject of proactive conservation measures by the Nevada Department of Wildlife and the U.S. Fish and Wildlife Service since 2008 due to concerns about potential habitat degradation resulting from exploitation of nearby geothermal energy resources. These toads appear to belong within the Anaxyrus boreas species group but are commonly referred to as Dixie Valley toads (DVTs). The DVT is currently confined to an extremely narrow habitat range (370 ha) that is geographically isolated from any other A. boreas population. In this study, genetic variations in mitochondrial genes and 11 microsatellite loci were used to assess the affinities of DVTs in relation to members of the A. boreas species group. We compared results from DVTs with previously published data spanning much of the range of A. boreas in the United States and new data from a nearby toad population within Dixie Valley. Data from both mitochondrial DNA and microsatellites placed DVTs inside the A. boreas species group. In particular, DVTs fell into a cluster of A. boreas from Washington and California, along with other species from the A. boreas species group, namely A. nelsoni, A. canorus, and A. exsul. Genetic differentiation of DVTs was lowest between A. boreas populations in Washington and California. However, allele frequencies were significantly different between DVTs and all other populations, including a nearby locality within Dixie Valley. This genetic differentiation, along with the DVT's geographical isolation and restricted habitat, warrants recognition of the DVT as a distinct management unit.

Nevada

Annotated bibliography of scientific research on Gunnison sage-grouse published from January 2005 to September 2022

Integrating recent scientific knowledge into management decisions supports effective natural resource management and can lead to better resource outcomes. However, finding and accessing scientific knowledge can be time consuming and costly. To assist in this process, the U.S. Geological Survey is creating a series of annotated bibliographies on topics of management concern for western lands. Previously published reports introduced a methodology for preparing annotated bibliographies to facilitate the integration of recent, peer-reviewed science into resource management decisions. Therefore, relevant text from those efforts is reproduced here to frame the presentation. Centrocercus minimus (Gunnison sage-grouse; hereafter GUSG) has been a focus of scientific investigation since the early 2000s. The U.S. Fish and Wildlife Service listed GUSG as threatened under the Endangered Species Act in 2014 because of declining populations and increasing habitat loss. The U.S. Fish and Wildlife Service, Bureau of Land Management, and Colorado Parks and Wildlife have sought to increase the conservation of this species by adapting management and recovery plans to reduce threats and increase population resiliency. GUSG are studied less than the closely related Centrocercus urophasianus (greater sage-grouse); however, research efforts have recently increased to understand the life history, genetics, and habitat suitability of this sagebrush-obligate species. We compiled and summarized peer-reviewed journal articles, data products, and formal technical reports (such as U.S. Department of Agriculture Forest Service General Technical Reports and U.S. Geological Survey Open-File Reports) on GUSG, published between January 2005 and September 2022. We first systematically searched three reference databases and three government databases using the following search phrases: “Gunnison sage-grouse” or “lesser sage-grouse” or “Gunnison grouse” or “Gunnison sage grouse” or “lesser sage grouse” or “ Centrocercus minimus .” We refined the initial list of products by removing (1) duplicates, (2) publications that were not published as research, data products, or scientific review articles in peer-reviewed journals or as formal technical reports, and (3) products that did not have GUSG as a research focus or products that did not present new data or findings about GUSG. We summarized each product using a consistent structure (background, objectives, methods, location, findings, and implications) and identified the management topics (for example, population estimates or targets, habitat, and management efforts) addressed by each product. We also noted which publications included new geospatial data. The review process for this annotated bibliography included two initial internal colleague reviews of each summary, requesting input on each summary from an author of the original publication, and a formal peer review. Our initial searches resulted in 80 total products, of which 63 met our criteria for inclusion of which 53 were products that had not been summarized before. Across products summarized in the annotated bibliography, broad-scale habitat characteristics; population estimates or targets; behavior or demographics; and genetics were the most commonly addressed management topics. The bibliographies are available on the Science for Resource Managers tool ( https://apps.usgs.gov/science-for-resource-managers ) and are searchable by topic, location, and year, and the search tool includes links to each original publication. The studies compiled and summarized in this annotated bibliography may inform planning and management actions that seek to maintain and restore sagebrush landscapes and GUSG populations across the GUSG range.

Colorado