A test of Conserving Nature's Stage: protecting a diversity of geophysical traits can also support a diversity of species at a landscape scale.

Conserving Nature's Stage (CNS) is a concept from conservation planning that promotes the protection of areas encompassing a broad range of enduring geophysical traits to provide long-term habitat for diverse species. The efficacy of using enduring geophysical characteristics as surrogates for biodiversity, independent of non-geophysical features and when considering finer resolution area selections, has yet to be investigated. Here, we evaluated CNS using 33 fine-scale inventories of vascular plant, non-vascular plant, invertebrate or vertebrate species from 13 areas across three continents. For each inventory, we estimated a continuous multidimensional surrogate defined from topographic and soil estimates of the surveyed plots. We assessed surrogate effectiveness by comparing the species representation of surrogate selected plots to the representation from plots picked randomly and using species information. We then used correlation coefficients to assess the link between the performance and qualities of the inventories, surroundings and surrogates. The CNS surrogate showed positive performance for 24 of the 33 inventories, and among these tests, represented 28 more species than random and 83% of the total number of species on average. We also found a small number of weak correlations between performance and environmental variability, as well as qualities of the surrogate. Our study demonstrates that prioritizing areas for a variety of geophysical characteristics will, in most cases, promote the representation of species. Our findings also point to areas for future research that might enhance CNS surrogacy. This article is part of the Theo Murphy meeting issue 'Geodiversity for science and society'.

The ecology of human-caused mortality for a protected large carnivore.

Mitigating human-caused mortality for large carnivores is a pressing global challenge for wildlife conservation. However, mortality is almost exclusively studied at local (within-population) scales creating a mismatch between our understanding of risk and the spatial extent most relevant to conservation and management of wide-ranging species. Here, we quantified mortality for 590 radio-collared mountain lions statewide across their distribution in California to identify drivers of human-caused mortality and investigate whether human-caused mortality is additive or compensatory. Human-caused mortality, primarily from conflict management and vehicles, exceeded natural mortality despite mountain lions being protected from hunting. Our data indicate that human-caused mortality is additive to natural mortality as population-level survival decreased as a function of increasing human-caused mortality and natural mortality did not decrease with increased human-caused mortality. Mortality risk increased for mountain lions closer to rural development and decreased in areas with higher proportions of citizens voting to support environmental initiatives. Thus, the presence of human infrastructure and variation in the mindset of humans sharing landscapes with mountain lions appear to be primary drivers of risk. We show that human-caused mortality can reduce population-level survival of large carnivores across large spatial scales, even when they are protected from hunting.

Enhanced regional connectivity between western North American national parks will increase persistence of mammal species diversity.

Many protected areas worldwide increasingly resemble habitat isolates embedded in human-modified landscapes. However, establishing linkages among protected areas could significantly reduce species-loss rates. Here we present a novel method having broad applicability for assessing enhanced regional connectivity on persistence of mammal diversity. We combine theoretically-derived species relaxation rates for mammal communities with empirically-derived pathways. We assess the value of enhanced regional connectivity for two hypothetical networks of national parks in western North America: the Yellowstone-Glacier network and the Mount Rainier-North Cascades network. Linking the Yellowstone and Glacier park assemblages by eliminating barriers to movement in identified mammal dispersal pathways and by incorporating adjacent wilderness areas and known ungulate migratory routes into a protected area network would greatly enlarge available habitat. This would enhance medium to large mammal species persistence time by factor of 4.3, on average, or ~ 682 generations relative to individual parks. Similarly, linking Mount Rainier and North Cascades park assemblages would enhance mammal species persistence time by a factor of 4.3, on average, or ~305 generations relative to individual parks. Enhancing regional connectivity among western North America parks could serve as an important template for landscape-scale conservation in the 21st century.

Identifying genetic relationships among tarsier populations in the islands of Bunaken National Park and mainland Sulawesi.

Eastern tarsiers (Tarsius tarsier complex) are small nocturnal primates endemic to Sulawesi Island and small adjacent islands of Indonesia. In 2004, the hybrid biogeography hypothesis predicted this species complex might contain 16 or more taxa, each corresponding to a region of endemism, based on: 1) geological evidence of the development of the archipelago, 2) biological evidence in the form of concordant distributions of monkeys and toads, and 3) the distribution of tarsier acoustic groups. Since then, 11 tarsier species have been recognized, potentially leaving more to be described. Efforts to identify these cryptic species are urgently needed so that habitat conversion, pet trade, and cultural activities will not render some species extinct before they are recognized. We gathered data to test the hypothesis of cryptic tarsier species on three volcanic islands in Bunaken National Park, North Sulawesi, namely Bunaken, Manadotua, and Mantehage, during May-August 2018. We sequenced individuals at 5 nuclear genes (ABCA1, ADORA3, AXIN1, RAG, and TTR) and made comparisons to existing genotypes at 14 mainland sites. Bayesian phylogenetic analyses revealed that island populations are genetically identical in all 5 genes, and formed a clade separated from the mainland ones. The eastern tarsiers first diverged from the western tarsiers approximately 2.5 MYA. The three island populations diverged from mainland tarsiers approximately 2,000-150,000 YA, due to either human activities or natural rafting. This study provides information for tarsier conservation, advances the understanding of biogeography of Sulawesi, and contributes to Indonesian awareness of biodiversity. Further quantitative genetics research on tarsiers, especially the island populations, will offer significant insights to establish more efficient and strategic tarsier conservation actions.

Extinction vortex dynamics of top predators isolated by urbanization.

Extinction risk is elevated in small, isolated populations due to demographic and genetic interactions. Therefore, it is critical to model these processes realistically in population viability analyses (PVA) to inform local management and contribute to a greater understanding of mechanisms within the extinction vortex. We conducted PVA's for two small mountain lion populations isolated by urbanization in southern California to predict population growth, extinction probability, and loss of genetic diversity with empirical data. Specifically, we (1) provide the first PVA for isolated mountain lions in the Santa Ana Mountains (SAM) that considers both demographic and genetic risk factors and (2) test the hypothesis that variation in abundance and mortality between the SAM and Santa Monica Mountains (SMM) result in differences in population growth, loss of heterozygosity, and extinction probability. Our models predicted 16-21% probability of local extinction in the SAM due purely to demographic processes over 50 yr with current low levels or no immigration. Our models also predicted that genetic diversity will further erode in the SAM such that concern regarding inbreeding depression is warranted unless gene flow is increased, and that if inbreeding depression occurs, rapid local extinction will be highly likely. Dynamics of the two populations were broadly similar, but they also exhibited differences driven by larger population size and higher mortality in the SAM. Density-independent scenarios predicted a rapidly increasing population in the SMM, whereas growth potential did not differ from a stable trend in the SAM. Demographic extinction probability and loss of heterozygosity were greater in the SMM for density-dependent scenarios without immigration. However, higher levels of immigration had stronger, positive influences on both demographic viability and retention of genetic diversity in the SMM driven by lower abundance and higher adult survival. Our results elucidate demographic and genetic threats to small populations within the extinction vortex, and how these vary relative to demographic structure. Importantly, simulating seemingly attainable increases in connectivity was sufficient to greatly reduce extinction probability. Our work highlights that conservation of large carnivores is achievable within urbanized landscapes, but requires land protection, connectivity, and strategies to promote coexistence with humans.

Circuit-theory applications to connectivity science and conservation.

Conservation practitioners have long recognized ecological connectivity as a global priority for preserving biodiversity and ecosystem function. In the early years of conservation science, ecologists extended principles of island biogeography to assess connectivity based on source patch proximity and other metrics derived from binary maps of habitat. From 2006 to 2008, the late Brad McRae introduced circuit theory as an alternative approach to model gene flow and the dispersal or movement routes of organisms. He posited concepts and metrics from electrical circuit theory as a robust way to quantify movement across multiple possible paths in a landscape, not just a single least-cost path or corridor. Circuit theory offers many theoretical, conceptual, and practical linkages to conservation science. We reviewed 459 recent studies citing circuit theory or the open-source software Circuitscape. We focused on applications of circuit theory to the science and practice of connectivity conservation, including topics in landscape and population genetics, movement and dispersal paths of organisms, anthropogenic barriers to connectivity, fire behavior, water flow, and ecosystem services. Circuit theory is likely to have an effect on conservation science and practitioners through improved insights into landscape dynamics, animal movement, and habitat-use studies and through the development of new software tools for data analysis and visualization. The influence of circuit theory on conservation comes from the theoretical basis and elegance of the approach and the powerful collaborations and active user community that have emerged. Circuit theory provides a springboard for ecological understanding and will remain an important conservation tool for researchers and practitioners around the globe.

Aplicaciones de la Teoría de Circuitos a la Conservación y a la Ciencia de la Conectividad Resumen Quienes practican la conservación han reconocido durante mucho tiempo que la conectividad ecológica es una prioridad mundial para la preservación de la biodiversidad y el funcionamiento del ecosistema. Durante los primeros años de la ciencia de la conservación los ecólogos difundieron los principios de la biografía de islas para evaluar la conectividad con base en la proximidad entre el origen y el fragmento, así como otras medidas derivadas de los mapas binarios de los hábitats. Entre 2006 y 2008 el fallecido Brad McRae introdujo la teoría de circuitos como una estrategia alternativa para modelar el flujo génico y la dispersión o las rutas de movimiento de los organismos. McRae propuso conceptos y medidas de la teoría de circuitos eléctricos como una manera robusta para cuantificar el movimiento a lo largo de múltiples caminos posibles en un paisaje, no solamente a lo largo de un camino o corredor de menor costo. La teoría de circuitos ofrece muchos enlaces teóricos, conceptuales y prácticos con la ciencia de la conservación. Revisamos 459 estudios recientes que citan la teoría de circuitos o el software de fuente abierta Circuitscape. Nos enfocamos en las aplicaciones de la teoría de circuitos a la ciencia y a la práctica de la conservación de la conectividad, incluyendo temas como la genética poblacional y del paisaje, movimiento y caminos de dispersión de los organismos, barreras antropogénicas de la conectividad, comportamiento ante incendios, flujo del agua, y servicios ambientales. La teoría de circuitos probablemente tenga un efecto sobre la ciencia de la conservación y quienes la practican por medio de una percepción mejorada de las dinámicas del paisaje, el movimiento animal, y los estudios de uso de hábitat, y por medio del desarrollo de nuevas herramientas de software para el análisis de datos y su visualización. La influencia de la teoría de circuitos sobre la conservación viene de la base teórica y la elegancia de la estrategia y de las colaboraciones fuertes y la comunidad activa de usuarios que han surgido recientemente. La teoría de circuitos proporciona un trampolín para el entendimiento ecológico y seguirá siendo una importante herramienta de conservación para los investigadores y practicantes en todo el mundo.

A tribute to a true conservation innovator, Brad McRae, 1966-2017.

Powerful innovations can occur when a concept is taken from one field and used to solve a problem in an unrelated field. In fact, it has been shown that as the distance between a problem solver's field of technical expertise and the focal field of a problem increase, so does the probability of success. This article is protected by copyright. All rights reserved.

Improving the use of environmental diversity as a surrogate for species representation.

The continuous p-median approach to environmental diversity (ED) is a reliable way to identify sites that efficiently represent species. A recently developed maximum dispersion (maxdisp) approach to ED is computationally simpler, does not require the user to reduce environmental space to two dimensions, and performed better than continuous p-median for datasets of South African animals. We tested whether maxdisp performs as well as continuous p-median for 12 datasets that included plants and other continents, and whether particular types of environmental variables produced consistently better models of ED. We selected 12 species inventories and atlases to span a broad range of taxa (plants, birds, mammals, reptiles, and amphibians), spatial extents, and resolutions. For each dataset, we used continuous p-median ED and maxdisp ED in combination with five sets of environmental variables (five combinations of temperature, precipitation, insolation, NDVI, and topographic variables) to select environmentally diverse sites. We used the species accumulation index (SAI) to evaluate the efficiency of ED in representing species for each approach and set of environmental variables. Maxdisp ED represented species better than continuous p-median ED in five of 12 biodiversity datasets, and about the same for the other seven biodiversity datasets. Efficiency of ED also varied with type of variables used to define environmental space, but no particular combination of variables consistently performed best. We conclude that maxdisp ED performs at least as well as continuous p-median ED, and has the advantage of faster and simpler computation. Surprisingly, using all 38 environmental variables was not consistently better than using subsets of variables, nor did any subset emerge as consistently best or worst; further work is needed to identify the best variables to define environmental space. Results can help ecologists and conservationists select sites for species representation and assist in conservation planning.

Predicted rarity-weighted richness, a new tool to prioritize sites for species representation.

Lack of biodiversity data is a major impediment to prioritizing sites for species representation. Because comprehensive species data are not available in any planning area, planners often use surrogates (such as vegetation communities, or mapped occurrences of a well-inventoried taxon) to prioritize sites. We propose and demonstrate the effectiveness of predicted rarity-weighted richness (PRWR) as a surrogate in situations where species inventories may be available for a portion of the planning area. Use of PRWR as a surrogate involves several steps. First, rarity-weighted richness (RWR) is calculated from species inventories for a q% subset of sites. Then random forest models are used to model RWR as a function of freely available environmental variables for that q% subset. This function is then used to calculate PRWR for all sites (including those for which no species inventories are available), and PRWR is used to prioritize all sites. We tested PRWR on plant and bird datasets, using the species accumulation index to measure efficiency of PRWR. Sites with the highest PRWR represented species with median efficiency of 56% (range 32%-77% across six datasets) when q = 20%, and with median efficiency of 39% (range 20%-63%) when q = 10%. An efficiency of 56% means that selecting sites in order of PRWR rank was 56% as effective as having full knowledge of species distributions in PRWR's ability to improve on the number of species represented in the same number of randomly selected sites. Our results suggest that PRWR may be able to help prioritize sites to represent species if a planner has species inventories for 10%-20% of the sites in the planning area.

Downscaling patterns of complementarity to a finer resolution and its implications for conservation prioritization.

Given species inventories of all sites in a planning area, integer programming or heuristic algorithms can prioritize sites in terms of the site's complementary value, that is, the ability of the site to complement (add unrepresented species to) other sites prioritized for conservation. The utility of these procedures is limited because distributions of species are typically available only as coarse atlases or range maps, whereas conservation planners need to prioritize relatively small sites. If such coarse-resolution information can be used to identify small sites that efficiently represent species (i.e., downscaled), then such data can be useful for conservation planning. We develop and test a new type of surrogate for biodiversity, which we call downscaled complementarity. In this approach, complementarity values from large cells are downscaled to small cells, using statistical methods or simple map overlays. We illustrate our approach for birds in Spain by building models at coarse scale (50 × 50 km atlas of European birds, and global range maps of birds interpreted at the same 50 × 50 km grid size), using this model to predict complementary value for 10 × 10 km cells in Spain, and testing how well-prioritized cells represented bird distributions in an independent bird atlas of those 10 × 10 km cells. Downscaled complementarity was about 63-77% as effective as having full knowledge of the 10-km atlas data in its ability to improve on random selection of sites. Downscaled complementarity has relatively low data acquisition cost and meets representation goals well compared with other surrogates currently in use. Our study justifies additional tests to determine whether downscaled complementarity is an effective surrogate for other regions and taxa, and at spatial resolution finer than 10 × 10 km cells. Until such tests have been completed, we caution against assuming that any surrogate can reliably prioritize sites for species representation.

Evaluating ß Diversity as a Surrogate for Species Representation at Fine Scale.

Species turnover or ß diversity is a conceptually attractive surrogate for conservation planning. However, there has been only 1 attempt to determine how well sites selected to maximize ß diversity represent species, and that test was done at a scale too coarse (2,500 km2 sites) to inform most conservation decisions. We used 8 plant datasets, 3 bird datasets, and 1 mammal dataset to evaluate whether sites selected to span ß diversity will efficiently represent species at finer scale (sites sizes < 1 ha to 625 km2). We used ordinations to characterize dissimilarity in species assemblages (ß diversity) among plots (inventory data) or among grid cells (atlas data). We then selected sites to maximize ß diversity and used the Species Accumulation Index, SAI, to evaluate how efficiently the surrogate (selecting sites for maximum ß diversity) represented species in the same taxon. Across all 12 datasets, sites selected for maximum ß diversity represented species with a median efficiency of 24% (i.e., the surrogate was 24% more effective than random selection of sites), and an interquartile range of 4% to 41% efficiency. ß diversity was a better surrogate for bird datasets than for plant datasets, and for atlas datasets with 10-km to 14-km grid cells than for atlas datasets with 25-km grid cells. We conclude that ß diversity is more than a mere descriptor of how species are distributed on the landscape; in particular ß diversity might be useful to maximize the complementarity of a set of sites. Because we tested only within-taxon surrogacy, our results do not prove that ß diversity is useful for conservation planning. But our results do justify further investigation to identify the circumstances in which ß diversity performs well, and to evaluate it as a cross-taxon surrogate.

Using abiotic variables to predict importance of sites for species representation.

In systematic conservation planning, species distribution data for all sites in a planning area are used to prioritize each site in terms of the site's importance toward meeting the goal of species representation. But comprehensive species data are not available in most planning areas and would be expensive to acquire. As a shortcut, ecologists use surrogates, such as occurrences of birds or another well-surveyed taxon, or land types defined from remotely sensed data, in the hope that sites that represent the surrogates also represent biodiversity. Unfortunately, surrogates have not performed reliably. We propose a new type of surrogate, predicted importance, that can be developed from species data for a q% subset of sites. With species data from this subset of sites, importance can be modeled as a function of abiotic variables available at no charge for all terrestrial areas on Earth. Predicted importance can then be used as a surrogate to prioritize all sites. We tested this surrogate with 8 sets of species data. For each data set, we used a q% subset of sites to model importance as a function of abiotic variables, used the resulting function to predict importance for all sites, and evaluated the number of species in the sites with highest predicted importance. Sites with the highest predicted importance represented species efficiently for all data sets when q = 25% and for 7 of 8 data sets when q = 20%. Predicted importance requires less survey effort than direct selection for species representation and meets representation goals well compared with other surrogates currently in use. This less expensive surrogate may be useful in those areas of the world that need it most, namely tropical regions with the highest biodiversity, greatest biodiversity loss, most severe lack of inventory data, and poorly developed protected area networks.

Environmental diversity as a surrogate for species representation.

Because many species have not been described and most species ranges have not been mapped, conservation planners often use surrogates for conservation planning, but evidence for surrogate effectiveness is weak. Surrogates are well-mapped features such as soil types, landforms, occurrences of an easily observed taxon (discrete surrogates), and well-mapped environmental conditions (continuous surrogate). In the context of reserve selection, the idea is that a set of sites selected to span diversity in the surrogate will efficiently represent most species. Environmental diversity (ED) is a rarely used surrogate that selects sites to efficiently span multivariate ordination space. Because it selects across continuous environmental space, ED should perform better than discrete surrogates (which necessarily ignore within-bin and between-bin heterogeneity). Despite this theoretical advantage, ED appears to have performed poorly in previous tests of its ability to identify 50 × 50 km cells that represented vertebrates in Western Europe. Using an improved implementation of ED, we retested ED on Western European birds, mammals, reptiles, amphibians, and combined terrestrial vertebrates. We also tested ED on data sets for plants of Zimbabwe, birds of Spain, and birds of Arizona (United States). Sites selected using ED represented European mammals no better than randomly selected cells, but they represented species in the other 7 data sets with 20% to 84% effectiveness. This far exceeds the performance in previous tests of ED, and exceeds the performance of most discrete surrogates. We believe ED performed poorly in previous tests because those tests considered only a few candidate explanatory variables and used suboptimal forms of ED's selection algorithm. We suggest future work on ED focus on analyses at finer grain sizes more relevant to conservation decisions, explore the effect of selecting the explanatory variables most associated with species turnover, and investigate whether nonclimate abiotic variables can provide useful surrogates in an ED framework.

A review of selection-based tests of abiotic surrogates for species representation.

Because conservation planners typically lack data on where species occur, environmental surrogates--including geophysical settings and climate types--have been used to prioritize sites within a planning area. We reviewed 622 evaluations of the effectiveness of abiotic surrogates in representing species in 19 study areas. Sites selected using abiotic surrogates represented more species than an equal number of randomly selected sites in 43% of tests (55% for plants) and on average improved on random selection of sites by about 8% (21% for plants). Environmental diversity (ED) (42% median improvement on random selection) and biotically informed clusters showed promising results and merit additional testing. We suggest 4 ways to improve performance of abiotic surrogates. First, analysts should consider a broad spectrum of candidate variables to define surrogates, including rarely used variables related to geographic separation, distance from coast, hydrology, and within-site abiotic diversity. Second, abiotic surrogates should be defined at fine thematic resolution. Third, sites (the landscape units prioritized within a planning area) should be small enough to ensure that surrogates reflect species' environments and to produce prioritizations that match the spatial resolution of conservation decisions. Fourth, if species inventories are available for some planning units, planners should define surrogates based on the abiotic variables that most influence species turnover in the planning area. Although species inventories increase the cost of using abiotic surrogates, a modest number of inventories could provide the data needed to select variables and evaluate surrogates. Additional tests of nonclimate abiotic surrogates are needed to evaluate the utility of conserving nature's stage as a strategy for conservation planning in the face of climate change.