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Climate-smart conservation: putting adaption principles into practice

Climate change already is having significant impacts on the nation’s species and ecosystems, and these effects are projected to increase considerably over time. As a result, climate change is now a primary lens through which conservation and natural resource management must be viewed. How should we prepare for and respond to the impacts of climate change on wildlife and their habitats? What should we be doing differently in light of these climatic shifts, and what actions continue to make sense? Climate-Smart Conservation: Putting Adaptation Principles into Practice offers guidance for designing and carrying out conservation in the face of a rapidly changing climate. Addressing the growing threats brought about or accentuated by rapid climate change requires a fundamental shift in the practice of natural resource management and conservation. Traditionally, conservationists have focused their efforts on protecting and managing systems to maintain their current state, or to restore degraded systems back to a historical state regarded as more desirable. Conservation planners and practitioners will need to adopt forward-looking goals and implement strategies specifically designed to prepare for and adjust to current and future climatic changes, and the associated impacts on natural systems and human communities—an emerging discipline known as climate change adaptation. The field of climate change adaptation is still in its infancy. Although there is increasing attention focused on the subject, much of the guidance developed to date has been general in nature, concentrating on high-level principles rather than specific actions. It is against this backdrop that this guide was prepared as a means for helping put adaptation principles into practice, and for moving adaptation from planning to action.

Report

Stewardship and management of freshwater ecosystems: From Leopold's land ethic to a freshwater ethic

In 1949, Aldo Leopold formalized the concept of the ‘land ethic’, in what emerged as a foundational and transformational way of thinking about natural resource management, biodiversity conservation, and stewardship in terrestrial systems. Yet, the land ethic has inherent linkages to aquatic ecosystems; Leopold himself conducted research on rivers and lakes, and freshwater ecosystems figured widely in his writing. We reflect on the land ethic and other aspects of Leopold's scholarship to identify key messages that provide insight into the stewardship and management of freshwater ecosystems around the globe. We also frame what we call the ‘freshwater ethic’ around Leopold's legacy. Although Leopold could not have envisaged the stressors affecting modern aquatic ecosystems, his core principles remain salient. These apply not only to ecosystem protection, but also to the ethics of modern conservation economics, sustainability, and the protection of natural capital, in which lakes, rivers, and wetlands now figure prominently. We identify key ‘Aldo-inspired’ recommendations for protecting and restoring freshwater ecosystems in the Anthropocene that emanate directly from his writings (e.g. adopt an ecosystem approach, identify win–win–win scenarios, recognize the irreplaceability of wild waters, and strive for freshwater optimism). In an epoch where links between people and nature are becoming more explicit in environmental management, policy, and governance, we suggest that Aldo Leopold's work illustrates how inspirational, seminal thinkers have offered leadership in this domain. We contend that today there is still much that can be learned from Leopold, especially by the next generation of environmental practitioners, to ensure the effective stewardship of our aquatic ecosystems. We submit that the adoption of a freshwater ethic in parallel with Leopold's land ethic will enhance the stewardship of the world's increasingly threatened fresh waters by raising the profile of the plight of fresh waters and identifying enduring actions that, if embraced, will help conserve and restore biodiversity.

Aquatic Conservation: Marine and Freshwater Ecosys

Predicting species distributions: unifying model selection and scale optimization for multi-scale occupancy models

Geographic distributions are a basic component of a species’ ecology, and predicting distributions is a fundamental task of conservation and resource management. Reliable prediction depends on identification of appropriate scales of effect for environmental data, and scale-optimization techniques are thus desirable to identify optimal scales for predictor variables. Recent statistical developments have also advanced methods of model selection based explicitly on predictive ability, which differ from commonly-used methods that regulate model structures via anticipated predictive performance. Such methods are beginning to permeate into species distribution models (SDMs), yet there remains no consensus methodology for developing optimally-predictive multi-scale SDMs when covariate data are collected over a range of scales. Thus, we compared the performance of common approaches for scale optimization and model selection in terms of their ability to produce optimally predictive multi-scale Bayesian occupancy models for predicting a species distribution, using models of the breeding distribution for King Rails (Rallus elegans) as a case study. Our results demonstrate sizable gains in predictive performance for hierarchical occupancy models selected explicitly via their ability to predict out-of-sample data using the logarithmic scoring rule, as compared to models selected using information criteria (DIC and WAIC). Information criteria commonly selected individual covariates, as well as scales of effect for those covariates, with suboptimal predictive performance. Performance of models selected using the logarithmic scoring rule was robust across method of scale optimization, which was not true for models selected using DIC and WAIC. Thus, we empirically demonstrate benefits of study designs that enable covariate and scale selection based explicitly on predictive ability. Our results also imply that more careful consideration of what constitutes an optimal scale is warranted in many ecological studies, as the meaning of optimal is not independent of the technique used for scale selection.

Ecosphere

Environmental DNA is an effective tool to track recolonizing migratory fish following large‐scale dam removal

Environmental DNA (eDNA) has emerged as a potentially powerful tool for use in conservation and resource management, including for tracking the recolonization dynamics of fish populations. We used eDNA to assess the effectiveness of dam removal to restore fish passage on the Elwha River in Washington State (USA). Using a suite of 11 species‐specific eDNA polymerase chain reaction (PCR) assays, we showed that most targeted anadromous species (five Pacific Salmon species and Pacific Lamprey) were able to pass upstream of both former dam sites. Multiscale occupancy modeling showed that the timing and spatial extent of recolonization differed among species during the four years of post‐dam removal monitoring. More abundant species like Chinook Salmon and Coho Salmon migrated farther into the upper portions of the watershed than less abundant species like Pink Salmon and Chum Salmon. Sampling also allowed assessment of potamodromous fish species. Bull Trout and Rainbow Trout, ubiquitous species in the watershed, were detected at all sampling locations. Environmental DNA from Brook Trout, a non‐native species isolated between the dams prior to dam removal, was detected downstream of Elwha dam but rarely upstream of the Glines Canyon Dam suggested that the species has not expanded its range appreciably in the watershed following dam removal. We found that eDNA was an effective tool to assess the response of fish populations to large‐scale dam removal on the Elwha River.

Environmental DNA

Ontogeny of eDNA shedding during early development in Chinook Salmon (Oncorhynchus tshawytscha)

Knowledge of the timing of major life history events in aquatic species is important for informing conservation and resource management planning. Accordingly, surveys of environmental DNA (eDNA) have been performed to determine the efficacy of eDNA for providing information on life history events, primarily focusing on the timing of events associated with spawning, and these studies have proved successful. However, spawning represents only one part of the life history, and therefore, information on eDNA shedding during other life history stages is needed to fill gaps in knowledge. Here, we explored eDNA shedding during early life history (from fertilized eggs until near yolk sac absorption) in Chinook Salmon ( Oncorhynchus tshawytscha ) at three biomasses in a laboratory environment. We found that fertilized eggs shed little eDNA prior to hatching. Hatching coincided with a spike in eDNA, and we observed a significant and positive relationship between eDNA concentration and the number of hatched eggs. The concentration of eDNA shed by larvae after hatching was not consistent across post-hatch sampling days, suggesting developmental and behavioral changes associated with larval ontogeny may affect eDNA shedding rate. These results indicate that eDNA data may be used to identify hatch timing and verify successful reproduction in oviparous aquatic fishes. The application of eDNA to early life history broadens the capacity of eDNA-based methods for assessing population status and trends.

Environmental DNA

How does climate change affect emergent properties of aquatic ecosystems?

Emergent properties of ecosystems are community attributes, such as structure and function, that arise from connections and interactions (e.g., predator–prey, competition) among populations, species, or assemblages that, when viewed together, provide a holistic representation that is more than the sum of its individual parts. Climate change is altering emergent properties of aquatic ecosystems through component responses, a combination of shifts in species range, phenology, distribution, and productivity, which lead to novel ecosystems that have no historical analog. The reshuffling, restructuring, and rewiring of aquatic ecosystems due to climate impacts are of high concern for natural resource management and conservation as these changes can lead to species extinctions and reductions in ecosystem services. Overall, we found that substantial progress has been made to advance our understanding of how climate change is affecting emergent properties of aquatic ecosystems. However, responses are incredibly complex, and high uncertainty remains for how systems will reorganize and function over the coming decades. This cross‐system perspective summarizes the state of knowledge of climate‐driven emergent properties in aquatic habitats with case studies that highlight mechanisms of change, observed or anticipated outcomes, as well as insights into confounding non‐climate effects, research tools, and management approaches to advance the field.

Fisheries

Topographic, bioclimatic, and vegetation characteristics of three ecoregion classification systems in North America: Comparisons along continent-wide transects

Ecoregion classification systems are increasingly used for policy and management decisions, particularly among conservation and natural resource managers. A number of ecoregion classification systems are currently available, with each system defining ecoregions using different classification methods and different types of data. As a result, each classification system describes a unique set of ecoregions. To help potential users choose the most appropriate ecoregion system for their particular application, we used three latitudinal transects across North America to compare the boundaries and environmental characteristics of three ecoregion classification systems [Ku??chler, World Wildlife Fund (WWF), and Bailey]. A variety of variables were used to evaluate the three systems, including woody plant species richness, normalized difference in vegetation index (NDVI), and bioclimatic variables (e.g., mean temperature of the coldest month) along each transect. Our results are dominated by geographic patterns in temperature, which are generally aligned north-south, and in moisture, which are generally aligned east-west. In the west, the dramatic changes in physiography, climate, and vegetation impose stronger controls on ecoregion boundaries than in the east. The Ku??chler system has the greatest number of ecoregions on all three transects, but does not necessarily have the highest degree of internal consistency within its ecoregions with regard to the bioclimatic and species richness data. In general, the WWF system appears to track climatic and floristic variables the best of the three systems, but not in all regions on all transects. ?? 2005 Springer Science+Business Media, Inc.

Environmental Management

Spatially explicit decision support for selecting translocation areas for Mojave desert tortoises

Spatially explicit decision support systems are assuming an increasing role in natural resource and conservation management. In order for these systems to be successful, however, they must address real-world management problems with input from both the scientific and management communities. The National Training Center at Fort Irwin, California, has expanded its training area, encroaching U.S. Fish and Wildlife Service critical habitat set aside for the Mojave desert tortoise ( Gopherus agassizii ), a federally threatened species. Of all the mitigation measures proposed to offset expansion, the most challenging to implement was the selection of areas most feasible for tortoise translocation. We developed an objective, open, scientifically defensible spatially explicit decision support system to evaluate translocation potential within the Western Mojave Recovery Unit for tortoise populations under imminent threat from military expansion. Using up to a total of 10 biological, anthropogenic, and/or logistical criteria, seven alternative translocation scenarios were developed. The final translocation model was a consensus model between the seven scenarios. Within the final model, six potential translocation areas were identified.

Biodiversity and Conservation

Spatial dynamics of ecosystem service flows: a comprehensive approach to quantifying actual services

Recent ecosystem services research has highlighted the importance of spatial connectivity between ecosystems and their beneficiaries. Despite this need, a systematic approach to ecosystem service flow quantification has not yet emerged. In this article, we present such an approach, which we formalize as a class of agent-based models termed “Service Path Attribution Networks” (SPANs). These models, developed as part of the Artificial Intelligence for Ecosystem Services (ARIES) project, expand on ecosystem services classification terminology introduced by other authors. Conceptual elements needed to support flow modeling include a service's rivalness, its flow routing type (e.g., through hydrologic or transportation networks, lines of sight, or other approaches), and whether the benefit is supplied by an ecosystem's provision of a beneficial flow to people or by absorption of a detrimental flow before it reaches them. We describe our implementation of the SPAN framework for five ecosystem services and discuss how to generalize the approach to additional services. SPAN model outputs include maps of ecosystem service provision, use, depletion, and flows under theoretical, possible, actual, inaccessible, and blocked conditions. We highlight how these different ecosystem service flow maps could be used to support various types of decision making for conservation and resource management planning.

Ecosystem Services

Forecasting water levels using the ConvLSTM algorithm in the Everglades, USA

Forecasting water levels in complex ecosystems like wetlands can support effective water resource management, ecological conservation, and understanding surface and groundwater hydrology. Predictive models can be used to simulate the complex interactions among natural processes, hydrometeorological factors, and human activities. The Greater Everglades in the USA is a well-known example of an ecosystem where complexity has motivated adoption of machine learning algorithms in water level prediction studies. This paper aims to contribute to extending existing machine learning algorithms by integrating spatiotemporal data with deep-learning algorithms in the forecasting process. In this study, a deep-learning model is developed to predict water levels on a regional scale, covering a large area of approximately 9,138 square kilometers in the Everglades ecosystem. This model has the architecture of Convolutional Long Short-Term Memory which can deal with spatiotemporal data by capturing both spatial and temporal dependencies in the training data. The forecasting capabilities of this model (referred to as the global model) are assessed by comparing the global model to two Artificial Neural Networks developed at two different gaging stations, referred to here as local models. One local model is developed at a gaging station directly influenced by nearby water control structures, whereas the other is developed at a gaging station located farther away from these structures. By leveraging data from the Everglades Depth Estimation Network spanning from January 2002 to May 2023, the global and local models were trained to forecast water levels with a two-day lead time. Our findings suggest that both the global and local models perform with approximately the same level of accuracy, with Mean Absolute Relative Error values ranging from 0.38% to 1.4% at the selected stations. The developed global model has demonstrated strong potential as a standalone forecasting tool for the entire study area in the Everglades and could eliminate the need for developing multiple local models. This finding also highlights how machine learning can capture complex spatial and temporal relationships to generate accurate water level predictions on a regional scale.

Florida

A science agenda to inform natural resource management decisions in an era of ecological transformation

Earth is experiencing widespread ecological transformation in terrestrial, freshwater, and marine ecosystems that is attributable to directional environmental changes, especially intensifying climate change. To better steward ecosystems facing unprecedented and lasting change, a new management paradigm is forming, supported by a decision-oriented framework that presents three distinct management choices: resist, accept, or direct the ecological trajectory. To make these choices strategically, managers seek to understand the nature of the transformation that could occur if change is accepted while identifying opportunities to intervene to resist or direct change. In this article, we seek to inspire a research agenda for transformation science that is focused on ecological and social science and based on five central questions that align with the resist–accept–direct (RAD) framework. Development of transformation science is needed to apply the RAD framework and support natural resource management and conservation on our rapidly changing planet.

BioScience

Tracking animals in freshwater with electronic tags: past, present and future

Considerable technical developments over the past half century have enabled widespread application of electronic tags to the study of animals in the wild, including in freshwater environments. We review the constraints associated with freshwater telemetry and biologging and the technical developments relevant to their use. Technical constraints for tracking animals are often influenced by the characteristics of the animals being studied and the environment they inhabit. Collectively, they influence which and how technologies can be used and their relative effectiveness. Although radio telemetry has historically been the most commonly used technology in freshwater, passive integrated transponder (PIT) technology, acoustic telemetry and biologgers are becoming more popular. Most telemetry studies have focused on fish, although an increasing number have focused on other taxa, such as turtles, crustaceans and molluscs. Key technical developments for freshwater systems include: miniaturization of tags for tracking small-size life stages and species, fixed stations and coded tags for tracking large samples of animals over long distances and large temporal scales, inexpensive PIT systems that enable mass tagging to yield population- and community-level relevant sample sizes, incorporation of sensors into electronic tags, validation of tag attachment procedures with a focus on maintaining animal welfare, incorporation of different techniques (for example, genetics, stable isotopes) and peripheral technologies (for example, geographic information systems, hydroacoustics), development of novel analytical techniques, and extensive international collaboration. Innovations are still needed in tag miniaturization, data analysis and visualization, and in tracking animals over larger spatial scales (for example, pelagic areas of lakes) and in challenging environments (for example, large dynamic floodplain systems, under ice). There seems to be a particular need for adapting various global positioning system and satellite tagging approaches to freshwater. Electronic tagging provides a mechanism to collect detailed information from imperilled animals and species that have no direct economic value. Current and future advances will continue to improve our knowledge of the natural history of aquatic animals and ecological processes in freshwater ecosystems while facilitating evidence-based resource management and conservation.

Animal Biotelemetry

Measurement of suction pressure dynamics of sea lampreys, Petromyzon marinus

Species-specific monitoring activities represent fundamental tools for natural resource management and conservation but require techniques that target species-specific traits or markers. Sea lamprey, a destructive invasive species in the Laurentian Great Lakes and conservation target in North America and Europe, is among very few fishes that possess and use oral suction, yet suction has not been exploited for sea lamprey control or conservation. Knowledge of specific characteristics of sea lamprey suction (e.g., amplitude, duration, and pattern of suction events; hereafter ‘suction dynamics’) may be useful to develop devices that detect, record, and respond to the presence of sea lamprey at a given place and time. Previous observations were limited to adult sea lampreys in static water. In this study, pressure sensing panels were constructed and used to measure oral suction pressures and describe suction dynamics of juvenile and adult sea lampreys at multiple locations within the mouth and in static and flowing water. Suction dynamics were largely consistent with previous descriptions, but more variation was observed. For adult sea lampreys, suction pressures ranged from –0.6 kPa to –26 kPa with 20 s to 200 s between pumps at rest, and increased to –8 kPa to –70 kPa when lampreys were manually disengaged. An array of sensors indicated that suction pressure distribution was largely uniform across the mouths of both juvenile and adult lampreys; but some apparent variation was attributed to obstruction of sensing portal holes by teeth. Suction pressure did not differ between static and flowing water when water velocity was lower than 0.45 m/s. Such information may inform design of new systems to monitor behavior, distribution and abundance of lampreys.

PLoS ONE

It's time for bold new approaches to link delta science and policymaking

California’s Sacramento–San Joaquin Delta is widely recognized as a highly damaged ecosystem. The Delta is also emblematic of a growing sense worldwide that society needs to do a better job of using scientific knowledge to guide conservation and resource management policies. Fortunately, we now have an unprecedented opportunity to get it right in building structures that support effective science–policy linkages in the Delta. By adopting bold steps to implement a “one Delta, one science” approach for a new Delta Science Plan, California can become a leading example of how to tackle the global problem of rapid ecological change and biodiversity loss. In this essay, we first describe the current paradox—continued environmental declines despite considerable investments in science and policy actions—and the high stakes of gambling with failure. Next, we explore why it is so hard to use scientific knowledge to design and implement policies that meet society’s sustainability goals. We then outline promising ways to overcome these obstacles, drawing on recent experiences. We conclude with thoughts on how to leverage this experience to develop a bold new approach to Delta science.

California

Stratigraphic section and selected semiquantitative chemistry, Meade Peak phosphatic shale member of Permian Phosphoria Formation, central part of Rasmussen Ridge, Caribou County, Idaho

The U.S. Geological Survey (USGS) has studied the Permian Phosphoria Formation in southeastern Idaho and the entire Western U.S. Phosphate Field throughout much of the twentieth century. In response to a request by the U.S. Bureau of Land Management, a new series of resource, geological, and geoenvironmental studies was undertaken by the USGS in 1998. To accomplish these studies, the USGS has formed cooperative research relationships with two Federal agencies, the Bureau of Land Management and the U.S. Forest Service, tasked with land management and resource conservation on public lands; and with five private companies currently leasing or developing phosphate resources in southeastern Idaho. The companies are Agrium U.S. Inc. (Rasmussen Ridge mine) , Astaris LLC (Dry Valley mine), Rhodia Inc. (Wooley Valley mine, inactive), J.R. Simplot Company (Smoky Canyon mine), and Monsanto Co. (Enoch Valley mine). Some of the mineralogical research associated with this project is supported through a cooperative agreement with the Department of Geology and Geological Enginee ring, University of Idaho. Present studies consist of integrated, multidisciplinary research directed toward (1) resource and reserve estimations of phosphate in selected 7.5-minute quadrangles; (2) elemental residence, mineralogical and petrochemical characteristics; (3) mobilization and reaction pathways, transport, and fate of potentially toxic elements associated with the occurrence, development, and societal use of phosphate; (4) geophysical signatures; and (5) improving the understanding of deposit origin. Because raw data acquired during the project will require time to interpret, the data are released in open-file reports for prompt availability to other workers. Open-file reports associated with this series of studies are submitted to each of the Federal and industry cooperators for comment; however, the USGS is solely responsible for the data contained in the reports.

Idaho

A New Map of Standardized Terrestrial Ecosystems of the Conterminous United States

A new map of standardized, mesoscale (tens to thousands of hectares) terrestrial ecosystems for the conterminous United States was developed by using a biophysical stratification approach. The ecosystems delineated in this top-down, deductive modeling effort are described in NatureServe's classification of terrestrial ecological systems of the United States. The ecosystems were mapped as physically distinct areas and were associated with known distributions of vegetation assemblages by using a standardized methodology first developed for South America. This approach follows the geoecosystems concept of R.J. Huggett and the ecosystem geography approach of R.G. Bailey. Unique physical environments were delineated through a geospatial combination of national data layers for biogeography, bioclimate, surficial materials lithology, land surface forms, and topographic moisture potential. Combining these layers resulted in a comprehensive biophysical stratification of the conterminous United States, which produced 13,482 unique biophysical areas. These were considered as fundamental units of ecosystem structure and were aggregated into 419 potential terrestrial ecosystems. The ecosystems classification effort preceded the mapping effort and involved the independent development of diagnostic criteria, descriptions, and nomenclature for describing expert-derived ecological systems. The aggregation and labeling of the mapped ecosystem structure units into the ecological systems classification was accomplished in an iterative, expert-knowledge-based process using automated rulesets for identifying ecosystems on the basis of their biophysical and biogeographic attributes. The mapped ecosystems, at a 30-meter base resolution, represent an improvement in spatial and thematic (class) resolution over existing ecoregionalizations and are useful for a variety of applications, including ecosystem services assessments, climate change impact studies, biodiversity conservation, and resource management.

Professional Paper

Evaluation and comparison of methods to estimate irrigation withdrawal for the National Water Census Focus Area Study of the Apalachicola-Chattahoochee-Flint River Basin in southwestern Georgia

Methods to estimate irrigation withdrawal using nationally available datasets and techniques that are transferable to other agricultural regions were evaluated by the U.S. Geological Survey as part of the Apalachicola-Chattahoochee-Flint (ACF) River Basin focus area study of the National Water Census (ACF–FAS). These methods investigated the spatial, temporal, and quantitative distributions of water withdrawal for irrigation in the southwestern Georgia region of the ACF–FAS, filling a vital need to inform science-based decisions regarding resource management and conservation. The crop– demand method assumed that only enough water is pumped onto a crop to satisfy the deficit between evapotranspiration and precipitation. A second method applied a geostatistical regimen of variography and conditional simulation to monthly metered irrigation withdrawal to estimate irrigation withdrawal where data do not exist. A third method analyzed Landsat satellite imagery using an automated approach to generate monthly estimates of irrigated lands. These methods were evaluated independently and compared collectively with measured water withdrawal information available in the Georgia part of the ACF–FAS, principally in the Chattahoochee-Flint River Basin. An assessment of each method’s contribution to the National Water Census program was also made to identify transfer value of the methods to the national program and other water census studies. None of the three methods evaluated represent a turnkey process to estimate irrigation withdrawal on any spatial (local or regional) or temporal (monthly or annual) extent. Each method requires additional information on agricultural practices during the growing season to complete the withdrawal estimation process. Spatial and temporal limitations inherent in identifying irrigated acres during the growing season, and in designing spatially and temporally representative monitor (meter) networks, can belie the ability of the methods to produce accurate irrigation-withdrawal estimates that can be used to produce dependable and consistent assessments of water availability and use for the National Water Census. Emerging satellite-data products and techniques for data analysis can generate high spatial-resolution estimates of irrigated-acres distributions with near-term temporal frequencies compatible with the needs of the ACF–FAS and the National Water Census.

Georgia

Calibrating environmental DNA metabarcoding to conventional surveys for measuring fish species richness

The ability to properly identify species present in a landscape is foundational to ecology and essential for natural resource management and conservation. However, many species are often unaccounted for due to ineffective direct capture and visual surveys, especially in aquatic environments. Environmental DNA metabarcoding is an approach that overcomes low detection probabilities and should consequently enhance estimates of biodiversity and its proxy, species richness. Here, we synthesize 37 studies in natural aquatic systems to compare species richness estimates for bony fish between eDNA metabarcoding and conventional methods, such as nets, visual census, and electrofishing. In freshwater systems with fewer than 100 species, we found eDNA metabarcoding detected more species than conventional methods. Using multiple genetic markers further increased species richness estimates with eDNA metabarcoding. For more diverse freshwater systems and across marine systems, eDNA metabarcoding reported similar values of species richness to conventional methods; however, more studies are needed in these environments to better evaluate relative performance. In systems with greater biodiversity, eDNA metabarcoding will require more populated reference databases, increased sampling effort, and multi-marker assays to ensure robust species richness estimates to further validate the approach. eDNA metabarcoding is reliable and provides a path for broader biodiversity assessments that can outperform conventional methods for estimating species richness.

Frontiers in Ecology and Evolution