Incorporating geodiversity into conservation decisions

In a rapidly changing climate, conservation practitioners could better use geodiversity in a broad range of conservation decisions. We explored selected avenues through which this integration might improve decision making and organized them within the adaptive management cycle of assessment, planning, implementation, and monitoring. Geodiversity is seldom referenced in predominant environmental law and policy. With most natural resource agencies mandated to conserve certain categories of species, agency personnel are challenged to find ways to practically implement new directives aimed at coping with climate change while retaining their species‐centered mandate. Ecoregions and ecological classifications provide clear mechanisms to consider geodiversity in plans or decisions, the inclusion of which will help foster the resilience of conservation to climate change. Methods for biodiversity assessment, such as gap analysis, climate change vulnerability analysis, and ecological process modeling, can readily accommodate inclusion of a geophysical component. We adapted others’ approaches for characterizing landscapes along a continuum of climate change vulnerability for the biota they support from resistant, to resilient, to susceptible, and to sensitive and then summarized options for integrating geodiversity into planning in each landscape type. In landscapes that are relatively resistant to climate change, options exist to fully represent geodiversity while ensuring that dynamic ecological processes can change over time. In more susceptible landscapes, strategies aiming to maintain or restore ecosystem resilience and connectivity are paramount. Implementing actions on the ground requires understanding of geophysical constraints on species and an increasingly nimble approach to establishing management and restoration goals. Because decisions that are implemented today will be revisited and amended into the future, increasingly sophisticated forms of monitoring and adaptation will be required to ensure that conservation efforts fully consider the value of geodiversity for supporting biodiversity in the face of a changing climate.     

Interacting Effects of Phenotypic Plasticity and Evolution on Population Persistence in a Changing Climate

Abstract: Climate change affects individual organisms by altering development, physiology, behavior, and fitness, and populations by altering genetic and phenotypic composition, vital rates, and dynamics. We sought to clarify how selection, phenotypic plasticity, and demography are linked in the context of climate change. On the basis of theory and results of recent empirical studies of plants and animals, we believe the ecological and evolutionary issues relevant to population persistence as climate changes are the rate, type, magnitude, and spatial pattern of climate‐induced abiotic and biotic change; generation time and life history of the organism; extent and type of phenotypic plasticity; amount and distribution of adaptive genetic variation across space and time; dispersal potential; and size and connectivity of subpopulations. An understanding of limits to plasticity and evolutionary potential across traits, populations, and species and feedbacks between adaptive and demographic responses is lacking. Integrated knowledge of coupled ecological and evolutionary mechanisms will increase understanding of the resilience and probabilities of persistence of populations and species.     

Incorporating Climate Science in Applications of the U.S. Endangered Species Act for Aquatic Species

Aquatic species are threatened by climate change but have received comparatively less attention than terrestrial species. We gleaned key strategies for scientists and managers seeking to address climate change in aquatic conservation planning from the literature and existing knowledge. We address 3 categories of conservation effort that rely on scientific analysis and have particular application under the U.S. Endangered Species Act (ESA): assessment of overall risk to a species; long‐term recovery planning; and evaluation of effects of specific actions or perturbations. Fewer data are available for aquatic species to support these analyses, and climate effects on aquatic systems are poorly characterized. Thus, we recommend scientists conducting analyses supporting ESA decisions develop a conceptual model that links climate, habitat, ecosystem, and species response to changing conditions and use this model to organize analyses and future research. We recommend that current climate conditions are not appropriate for projections used in ESA analyses and that long‐term projections of climate‐change effects provide temporal context as a species‐wide assessment provides spatial context. In these projections, climate change should not be discounted solely because the magnitude of projected change at a particular time is uncertain when directionality of climate change is clear. Identifying likely future habitat at the species scale will indicate key refuges and potential range shifts. However, the risks and benefits associated with errors in modeling future habitat are not equivalent. The ESA offers mechanisms for increasing the overall resilience and resistance of species to climate changes, including establishing recovery goals requiring increased genetic and phenotypic diversity, specifying critical habitat in areas not currently occupied but likely to become important, and using adaptive management. Incorporación de las Ciencias Climáticas en las Aplicaciones del Acta Estadunidense de Especies en Peligro para Especies Acuáticas     

Securing the Demographic and Genetic Future of Tuatara through Assisted Colonization

Abstract: Climate change poses a particular threat to species with fragmented distributions and little or no capacity to migrate. Assisted colonization, moving species into regions where they have not previously occurred, aims to establish populations where they are expected to survive as climatic envelopes shift. However, adaptation to the source environment may affect whether species successfully establish in new regions. Assisted colonization has spurred debate among conservation biologists and ecologists over whether the potential benefits to the threatened species outweigh the potential disruption to recipient communities. In our opinion, the debate has been distracted by controversial examples, rather than cases where assisted colonization may be a viable strategy. We present a strategic plan for the assisted migration of tuatara (Sphenodon punctatus), an endemic New Zealand reptile. The plan includes use of extant populations as reference points for comparisons with assisted‐colonization populations with respect to demography, phenotypic plasticity, and phenology; optimization of genetic variation; research to fill knowledge gaps; consideration of host and recipient communities; and inclusion of stakeholders in the planning stage. When strategically planned and monitored, assisted colonization could meet conservation and research goals and ultimately result in the establishment of long‐term sustainable populations capable of persisting during rapid changes in climate.     

Targeted gene flow for conservation

Anthropogenic threats often impose strong selection on affected populations, causing rapid evolutionary responses. Unfortunately, these adaptive responses are rarely harnessed for conservation. We suggest that conservation managers pay close attention to adaptive processes and geographic variation, with an eye to using them for conservation goals. Translocating pre‐adapted individuals into recipient populations is currently considered a potentially important management tool in the face of climate change. Targeted gene flow, which involves moving individuals with favorable traits to areas where these traits would have a conservation benefit, could have a much broader application in conservation. Across a species’ range there may be long‐standing geographic variation in traits or variation may have rapidly developed in response to a threatening process. Targeted gene flow could be used to promote natural resistance to threats to increase species resilience. We suggest that targeted gene flow is a currently underappreciated strategy in conservation that has applications ranging from the management of invasive species and their impacts to controlling the impact and virulence of pathogens.     

The Potential Conservation Value of Non‐Native Species

Abstract: Non‐native species can cause the loss of biological diversity (i.e., genetic, species, and ecosystem diversity) and threaten the well‐being of humans when they become invasive. In some cases, however, they can also provide conservation benefits. We examined the ways in which non‐native species currently contribute to conservation objectives. These include, for example, providing habitat or food resources to rare species, serving as functional substitutes for extinct taxa, and providing desirable ecosystem functions. We speculate that non‐native species might contribute to achieving conservation goals in the future because they may be more likely than native species to persist and provide ecosystem services in areas where climate and land use are changing rapidly and because they may evolve into new and endemic taxa. The management of non‐native species and their potential integration into conservation plans depends on how conservation goals are set in the future. A fraction of non‐native species will continue to cause biological and economic damage, and substantial uncertainty surrounds the potential future effects of all non‐native species. Nevertheless, we predict the proportion of non‐native species that are viewed as benign or even desirable will slowly increase over time as their potential contributions to society and to achieving conservation objectives become well recognized and realized.     

Using environmental and geographic data to optimize ex situ collections and preserve evolutionary potential

Maintenance of biodiversity through seed banks and botanical gardens, where the wealth of species’ genetic variation may be preserved ex situ, is a major goal of conservation. However, challenges can persist in optimizing ex situ collections if trade-offs exist among cost, effort, and conserving species evolutionary potential, particularly when genetic data are not available. We evaluated the genetic consequences of population preservation informed by geographic (isolation by distance [IBD]) and environmental (isolation by environment [IBE]) distance for ex situ collections for which population provenance is available. We used 19 genetic and genomic data sets from 15 plant species to assess the proportion of population genetic differentiation explained by geographic and environmental factors and to simulate ex situ collections prioritizing source populations based on pairwise geographic distance, environmental distance, or both. Specifically, we tested the impact prioritizing sampling based on these distances may have on the capture of neutral, functional, or putatively adaptive genetic diversity and differentiation. Individually, IBD and IBE explained limited population genetic differences across all 3 genetic marker classes (IBD, 10–16%; IBE, 1–5.5%). Together, they explained a substantial proportion of population genetic differences for functional (45%) and adaptive (71%) variation. Simulated ex situ collections revealed that inclusion of IBD, IBE, or both increased allelic diversity and genetic differentiation captured among populations, particularly for loci that may be important for adaptation. Thus, prioritizing population collections based on environmental and geographic distance data can optimize genetic variation captured ex situ. For the vast majority of plant species for which there is no genetic information, these data are invaluable to conservation because they can guide preservation of genetic variation needed to maintain evolutionary potential within collections.     

Conservation and Adaptation to Climate Change

Abstract: The need to adapt to climate change has become increasingly apparent, and many believe the practice of biodiversity conservation will need to alter to face this challenge. Conservation organizations are eager to determine how they should adapt their practices to climate change. This involves asking the fundamental question of what adaptation to climate change means. Most studies on climate change and conservation, if they consider adaptation at all, assume it is equivalent to the ability of species to adapt naturally to climate change as stated in Article 2 of the United Nations Framework Convention on Climate Change. Adaptation, however, can refer to an array of activities that range from natural adaptation, at one end of the spectrum, to sustainability science in coupled human and natural systems at the other. Most conservation organizations deal with complex systems in which adaptation to climate change involves making decisions on priorities for biodiversity conservation in the face of dynamic risks and involving the public in these decisions. Discursive methods such as analytic deliberation are useful for integrating scientific knowledge with public perceptions and values, particularly when large uncertainties and risks are involved. The use of scenarios in conservation planning is a useful way to build shared understanding at the science–policy interface. Similarly, boundary organizations—organizations or institutions that bridge different scales or mediate the relationship between science and policy—could prove useful for managing the transdisciplinary nature of adaptation to climate change, providing communication and brokerage services and helping to build adaptive capacity. The fact that some nongovernmental organizations (NGOs) are active across the areas of science, policy, and practice makes them well placed to fulfill this role in integrated assessments of biodiversity conservation and adaptation to climate change.     

Applying assessments of adaptive capacity to inform natural-resource management in a changing climate

Adaptive capacity (AC)—the ability of a species to cope with or accommodate climate change—is a critical determinant of species vulnerability. Using information on species’ AC in conservation planning is key to ensuring successful outcomes. We identified connections between a list of species’ attributes (e.g., traits, population metrics, and behaviors) that were recently proposed for assessing species’ AC and management actions that may enhance AC for species at risk of extinction. Management actions were identified based on evidence from the literature, a review of actions used in other climate adaptation guidance, and our collective experience in diverse fields of global-change ecology and climate adaptation. Selected management actions support the general AC pathways of persist in place or shift in space, in response to contemporary climate change. Some actions, such as genetic manipulations, can be used to directly alter the ability of species to cope with climate change, whereas other actions can indirectly enhance AC by addressing ecological or anthropogenic constraints on the expression of a species’ innate abilities to adapt. Ours is the first synthesis of potential management actions directly linked to AC. Focusing on AC attributes helps improve understanding of how and why aspects of climate are affecting organisms, as well as the mechanisms by which management interventions affect a species’ AC and climate change vulnerability. Adaptive-capacity-informed climate adaptation is needed to build connections among the causes of vulnerability, AC, and proposed management actions that can facilitate AC and reduce vulnerability in support of evolving conservation paradigms.     

Incorporating evolutionary processes into population viability models

We examined how ecological and evolutionary (eco‐evo) processes in population dynamics could be better integrated into population viability analysis (PVA). Complementary advances in computation and population genomics can be combined into an eco‐evo PVA to offer powerful new approaches to understand the influence of evolutionary processes on population persistence. We developed the mechanistic basis of an eco‐evo PVA using individual‐based models with individual‐level genotype tracking and dynamic genotype–phenotype mapping to model emergent population‐level effects, such as local adaptation and genetic rescue. We then outline how genomics can allow or improve parameter estimation for PVA models by providing genotypic information at large numbers of loci for neutral and functional genome regions. As climate change and other threatening processes increase in rate and scale, eco‐evo PVAs will become essential research tools to evaluate the effects of adaptive potential, evolutionary rescue, and locally adapted traits on persistence.     

Transforming ecology and conservation biology through genome editing

As the conservation challenges increase, new approaches are needed to help combat losses in biodiversity and slow or reverse the decline of threatened species. Genome-editing technology is changing the face of modern biology, facilitating applications that were unimaginable only a decade ago. The technology has the potential to make significant contributions to the fields of evolutionary biology, ecology, and conservation, yet the fear of unintended consequences from designer ecosystems containing engineered organisms has stifled innovation. To overcome this gap in the understanding of what genome editing is and what its capabilities are, more research is needed to translate genome-editing discoveries into tools for ecological research. Emerging and future genome-editing technologies include new clustered regularly interspaced short palindromic repeats (CRISPR) targeted sequencing and nucleic acid detection approaches as well as species genetic barcoding and somatic genome-editing technologies. These genome-editing tools have the potential to transform the environmental sciences by providing new noninvasive methods for monitoring threatened species or for enhancing critical adaptive traits. A pioneering effort by the conservation community is required to apply these technologies to real-world conservation problems.     

Comparison of conservation metrics in a case study of lemurs

Conservation planning is important to protect species from going extinct now that natural habitats are decreasing owing to human activity and climate change. However, there is considerable controversy in choosing appropriate metrics to weigh the value of species and geographic regions. For example, the added value of phylogenetic conservation‐selection criteria remains disputed because high correlations between them and the nonphylogenetic criteria of species richness have been reported. We evaluated the commonly used conservation metrics species richness, endemism, phylogenetic diversity (PD), and phylogenetic endemism (PE) in a case study on lemurs of Madagascar. This enabled us to identify the conservation target of each metric and consider how they may be used in future conservation planning. We also devised a novel metric that uses a phylogeny scaled according to the rate of phenotypic evolution as a proxy for a species’ ability to adapt to change. High rates of evolution may indicate generalization or specialization. Both specialization and low rates of evolution may result in an inability to adapt to changing environments. We examined conservation priorities by using the inverse of the rate of body mass evolution to account for species with low rates of evolution. In line with previous work, we found high correlations among species richness and PD (r = 0.96), and endemism and PE (r = 0.82) in Malagasy lemurs. Phylogenetic endemism in combination with rates of evolution and their inverse prioritized grid cells containing highly endemic and specialized lemurs at risk of extinction, such as Avahi occidentalis and Lepilemur edwardsi, 2 endangered lemurs with high rates of phenotypic evolution and low‐quality diets, and Hapalemur aureus, a critically endangered species with a low rate of body mass evolution and a diet consisting of very high doses of cyanide.     

Facilitating climate‐change‐induced range shifts across continental land‐use barriers

Climate changes impose requirements for many species to shift their ranges to remain within environmentally tolerable areas, but near‐continuous regions of intense human land use stretching across continental extents diminish dispersal prospects for many species. We reviewed the impact of habitat loss and fragmentation on species’ abilities to track changing climates and existing plans to facilitate species dispersal in response to climate change through regions of intensive land uses, drawing on examples from North America and elsewhere. We identified an emerging analytical framework that accounts for variation in species' dispersal capacities relative to both the pace of climate change and habitat availability. Habitat loss and fragmentation hinder climate change tracking, particularly for specialists, by impeding both propagule dispersal and population growth. This framework can be used to identify prospective modern‐era climatic refugia, where the pace of climate change has been slower than surrounding areas, that are defined relative to individual species' needs. The framework also underscores the importance of identifying and managing dispersal pathways or corridors through semi‐continental land use barriers that can benefit many species simultaneously. These emerging strategies to facilitate range shifts must account for uncertainties around population adaptation to local environmental conditions. Accounting for uncertainties in climate change and dispersal capabilities among species and expanding biological monitoring programs within an adaptive management paradigm are vital strategies that will improve species' capacities to track rapidly shifting climatic conditions across landscapes dominated by intensive human land use.     

Transforming conservation science and practice for a postnormal world

We examine issues to consider when reframing conservation science and practice in the context of global change. New framings of the links between ecosystems and society are emerging that are changing peoples’ values and expectations of nature, resulting in plural perspectives on conservation. Reframing conservation for global change can thus be regarded as a stage in the evolving relationship between people and nature rather than some recent trend. New models of how conservation links with transformative adaptation include how decision contexts for conservation can be reframed and integrated with an adaptation pathways approach to create new options for global‐change‐ready conservation. New relationships for conservation science and governance include coproduction of knowledge that supports social learning. New processes for implementing adaptation for conservation outcomes include deliberate practices used to develop new strategies, shift world views, work with conflict, address power and intergenerational equity in decisions, and build consciousness and creativity that empower agents to act. We argue that reframing conservation for global change requires scientists and practitioners to implement approaches unconstrained by discipline and sectoral boundaries, geopolitical polarities, or technical problematization. We consider a stronger focus on inclusive creation of knowledge and the interaction of this knowledge with societal values and rules is likely to result in conservation science and practice that meets the challenges of a postnormal world.     

Case studies of conservation plans that incorporate geodiversity

Geodiversity has been used as a surrogate for biodiversity when species locations are unknown, and this utility can be extended to situations where species locations are in flux. Recently, scientists have designed conservation networks that aim to explicitly represent the range of geophysical environments, identifying a network of physical stages that could sustain biodiversity while allowing for change in species composition in response to climate change. Because there is no standard approach to designing such networks, we compiled 8 case studies illustrating a variety of ways scientists have approached the challenge. These studies show how geodiversity has been partitioned and used to develop site portfolios and connectivity designs; how geodiversity‐based portfolios compare with those derived from species and communities; and how the selection and combination of variables influences the results. Collectively, they suggest 4 key steps when using geodiversity to augment traditional biodiversity‐based conservation planning: create land units from species‐relevant variables combined in an ecologically meaningful way; represent land units in a logical spatial configuration and integrate with species locations when possible; apply selection criteria to individual sites to ensure they are appropriate for conservation; and develop connectivity among sites to maintain movements and processes. With these considerations, conservationists can design more effective site portfolios to ensure the lasting conservation of biodiversity under a changing climate.     

Connecting today's climates to future climate analogs to facilitate movement of species under climate change

Increasing connectivity is an important strategy for facilitating species range shifts and maintaining biodiversity in the face of climate change. To date, however, few researchers have included future climate projections in efforts to prioritize areas for increasing connectivity. We identified key areas likely to facilitate climate‐induced species’ movement across western North America. Using historical climate data sets and future climate projections, we mapped potential species’ movement routes that link current climate conditions to analogous climate conditions in the future (i.e., future climate analogs) with a novel moving‐window analysis based on electrical circuit theory. In addition to tracing shifting climates, the approach accounted for landscape permeability and empirically derived species’ dispersal capabilities. We compared connectivity maps generated with our climate‐change‐informed approach with maps of connectivity based solely on the degree of human modification of the landscape. Including future climate projections in connectivity models substantially shifted and constrained priority areas for movement to a smaller proportion of the landscape than when climate projections were not considered. Potential movement, measured as current flow, decreased in all ecoregions when climate projections were included, particularly when dispersal was limited, which made climate analogs inaccessible. Many areas emerged as important for connectivity only when climate change was modeled in 2 time steps rather than in a single time step. Our results illustrate that movement routes needed to track changing climatic conditions may differ from those that connect present‐day landscapes. Incorporating future climate projections into connectivity modeling is an important step toward facilitating successful species movement and population persistence in a changing climate.     

Connectivity Planning to Address Climate Change

As the climate changes, human land use may impede species from tracking areas with suitable climates. Maintaining connectivity between areas of different temperatures could allow organisms to move along temperature gradients and allow species to continue to occupy the same temperature space as the climate warms. We used a coarse‐filter approach to identify broad corridors for movement between areas where human influence is low while simultaneously routing the corridors along present‐day spatial gradients of temperature. We modified a cost–distance algorithm to model these corridors and tested the model with data on current land‐use and climate patterns in the Pacific Northwest of the United States. The resulting maps identified a network of patches and corridors across which species may move as climates change. The corridors are likely to be robust to uncertainty in the magnitude and direction of future climate change because they are derived from gradients and land‐use patterns. The assumptions we applied in our model simplified the stability of temperature gradients and species responses to climate change and land use, but the model is flexible enough to be tailored to specific regions by incorporating other climate variables or movement costs. When used at appropriate resolutions, our approach may be of value to local, regional, and continental conservation initiatives seeking to promote species movements in a changing climate. Planificación de Conectividad para Atender el Cambio Climático     

Multispecies genetic objectives in spatial conservation planning

Growing threats to biodiversity and global alteration of habitats and species distributions make it increasingly necessary to consider evolutionary patterns in conservation decision making. Yet, there is no clear‐cut guidance on how genetic features can be incorporated into conservation‐planning processes, despite multiple molecular markers and several genetic metrics for each marker type to choose from. Genetic patterns differ between species, but the potential tradeoffs among genetic objectives for multiple species in conservation planning are currently understudied. We compared spatial conservation prioritizations derived from 2 metrics of genetic diversity (nucleotide and haplotype diversity) and 2 metrics of genetic isolation (private haplotypes and local genetic differentiation) in mitochondrial DNA of 5 marine species. We compared outcomes of conservation plans based only on habitat representation with plans based on genetic data and habitat representation. Fewer priority areas were selected for conservation plans based solely on habitat representation than on plans that included habitat and genetic data. All 4 genetic metrics selected approximately similar conservation‐priority areas, which is likely a result of prioritizing genetic patterns across a genetically diverse array of species. Largely, our results suggest that multispecies genetic conservation objectives are vital to creating protected‐area networks that appropriately preserve community‐level evolutionary patterns.     

The immediate costs and long-term benefits of assisted gene flow in large populations

With the genetic health of many plant and animal populations deteriorating due to climate change outpacing adaptation, interventions, such as assisted gene flow (AGF), may provide genetic variation necessary for populations to adapt to climate change. We ran genetic simulations to mimic different AGF scenarios in large populations and measured their outcomes on population-level fitness to determine circumstances in which it is worthwhile to perform AGF. In the absence of inbreeding depression, AGF was beneficial within a few generations only when introduced genotypes had much higher fitness than local individuals and traits affecting fitness were controlled by a few genes of large effect. AGF was harmful over short periods (e.g., first ∼10–20 generations) if there was strong outbreeding depression or introduced deleterious genetic variation. When the adaptive trait was controlled by many loci of small effect, the benefits of AGF took over 10 generations to realize—potentially too long for most climate-related management scenarios. The genomic integrity of the recipient population typically remained intact following AGF; the amount of genetic material from the donor population usually constituted no more of the recipient population's genome than the fraction of the population introduced. Significant genomic turnover (e.g., >50% replacement) only occurred when the selective advantage of the adaptive trait and translocation fraction were extremely high. Our results will be useful when adaptive management is used to maintain the genetic health and productivity of large populations under climate change.