Effect of hybridization with genome exclusion on extinction risk

Human‐induced habitat changes may lead to the breakdown of reproductive barriers between distantly related species. This phenomenon may result in fertile first‐generation hybrids (F₁) that exclude the genome of one parental species during gametogenesis, thus disabling introgression. The species extinction risk associated with hybridization with genome exclusion is largely underappreciated because the phenomenon produces only F₁ hybrid phenotype, leading to the misconception that hybrids are sterile and potentially of minor conservation concern. We used a simulation model that integrates the main genetic, demographic, and ecological processes to examine the dynamics of hybridization with genome exclusion. We showed that this mode of hybridization may lead to extremely rapid extinction when the process of genome exclusion is unbalanced between the interbreeding species and when the hybridization rate is not negligible. The coexistence of parental species was possible in some cases of asymmetrical genome exclusion, but show this equilibrium was highly vulnerable to environmental variation. Expanding the exclusive habitat of the species at risk allowed its persistence. Our results highlight the extent of possible extinction risk due to hybridization with genome exclusion and suggest habitat management as a promising conservation strategy. In anticipation of serious threats to biodiversity due to hybridization with genome exclusion, we recommend a detailed assessment of the reproductive status of hybrids in conservation programs. We suggest such assessments include the inspection of genetic content in hybrid gametes.     

Public views about editing genes in wildlife for conservation

Developments in CRISPR-based gene-editing technologies have generated a growing number of proposals to edit genes in wildlife to meet conservation goals. As these proposals have attracted greater attention, controversies have emerged among scientists and stakeholder groups over potential consequences and ethical implications of gene editing. Responsible governance cannot occur without consulting broader publics, yet little effort has been made to systematically assess public understandings and beliefs in relation to this new area of applied genetic engineering. We analyzed data from a survey of U.S. adults (n = 1600), collected by YouGov, and that examined respondents’ concerns about gene editing in animal and plant wildlife and how those concerns are shaped by cultural dispositions toward science and beliefs about the appropriateness of intervening in nature at the genetic level. On average, respondents perceived more risk than benefit in using these tools. Over 70% agreed that gene editing in wildlife could be “easily used for the wrong purposes.” When evaluating the moral acceptability of gene editing in wildlife, respondents evaluated applications to improve survival in endangered wildlife as more morally acceptable than applications to decrease abundance in a population or eliminate a population. Belief in the authority of scientific knowledge was positively related to favorable views of the benefits, risks, and moral acceptability of editing genes in wildlife. The belief that editing genes in wildlife inappropriately intervenes in nature predicted relatively more concern about risks and moral acceptability and skepticism about benefits. Given high levels of concern and skepticism about gene editing in wildlife for conservation among the U.S. public, a take-it-slow approach to making decisions about when or whether to use these tools is advisable. Early opinions, including those uncovered in this study, are likely to be provisional. Thus, consulting the public should be an ongoing process.     

Hierarchical Bayesian Spatial Models for Multispecies Conservation Planning and Monitoring

Abstract: Biologists who develop and apply habitat models are often familiar with the statistical challenges posed by their data's spatial structure but are unsure of whether the use of complex spatial models will increase the utility of model results in planning. We compared the relative performance of nonspatial and hierarchical Bayesian spatial models for three vertebrate and invertebrate taxa of conservation concern (Church's sideband snails [Monadenia churchi], red tree voles [Arborimus longicaudus], and Pacific fishers [Martes pennanti pacifica]) that provide examples of a range of distributional extents and dispersal abilities. We used presence–absence data derived from regional monitoring programs to develop models with both landscape and site‐level environmental covariates. We used Markov chain Monte Carlo algorithms and a conditional autoregressive or intrinsic conditional autoregressive model framework to fit spatial models. The fit of Bayesian spatial models was between 35 and 55% better than the fit of nonspatial analogue models. Bayesian spatial models outperformed analogous models developed with maximum entropy (Maxent) methods. Although the best spatial and nonspatial models included similar environmental variables, spatial models provided estimates of residual spatial effects that suggested how ecological processes might structure distribution patterns. Spatial models built from presence–absence data improved fit most for localized endemic species with ranges constrained by poorly known biogeographic factors and for widely distributed species suspected to be strongly affected by unmeasured environmental variables or population processes. By treating spatial effects as a variable of interest rather than a nuisance, hierarchical Bayesian spatial models, especially when they are based on a common broad‐scale spatial lattice (here the national Forest Inventory and Analysis grid of 24 km² hexagons), can increase the relevance of habitat models to multispecies conservation planning.     

Recovery of insular seabird populations years after rodent eradication

Seabirds have been particularly affected by invasive non-native species, which has led to the implementation of numerous eradication campaigns for the conservation of these keystone and highly vulnerable species. Although the benefits of eradication of invasive non-native species for seabird conservation have been demonstrated, the recovery kinetics of different seabird populations on islands after eradication remains poorly evaluated. We conducted long-term monitoring of the number of breeding pairs of seven seabird species on a small atoll, Surprise Island, New Caledonia (southwestern tropical Pacific). Marine avifauna of the island were surveyed yearly 4 years before to 4 years after rodent eradication (conducted in 2005), and we conducted multiple one-time surveys from ∼10 years before and ∼15 years after eradication. We sought to determine how different seabird species responded to the eradication of invasive rodents in an insular environment. Three species responded positively (two- to 10-fold increase in population size) to eradication with differences in lag time and sensitivity. The number of breeding pairs increased (effect sizes = 0.49–0.95 and 0.35–0.52) for two species over 4 years post-eradication due to immigration. One species had a longer (at least 5 years) response time than all others; breeding pairs increased for over 10 years after eradication. Long-term sampling was necessary to observe the responses of the seabird populations on the island because of the delayed response of a species to eradication not visible in the first years after eradication. Our results confirmed the positive effects of eradication of invasive non-native species on seabirds and emphasize the importance of mid- and long-term pre- and posteradication surveys to decipher the mechanisms of seabird recovery and confirm the benefits of eradication for conservation purposes.     

Contrasting ecological information content in whaling archives with modern cetacean surveys for conservation planning and identification of historical distribution changes

Many species are restricted to a marginal or suboptimal fraction of their historical range due to anthropogenic impacts, making it hard to interpret their ecological preferences from modern-day data alone. However, inferring past ecological states is limited by the availability of robust data and biases in historical archives, posing a challenge for policy makers . To highlight how historical records can be used to understand the ecological requirements of threatened species and inform conservation, we investigated sperm whale (Physeter macrocephalus) distribution in the Western Indian Ocean. We assessed differences in information content and habitat suitability predictions based on whale occurrence data from Yankee whaling logs (1792–1912) and from modern cetacean surveys (1995–2020). We built maximum entropy habitat suitability models containing static (bathymetry-derived) variables to compare models comprising historical-only and modern-only data. Using both historical and modern habitat suitability predictions  we assessed marine protected area (MPA) placement by contrasting suitability in- and outside MPAs. The historical model predicted high habitat suitability in shelf and coastal regions near continents and islands, whereas the modern model predicted a less coastal distribution with high habitat suitability more restricted to areas of steep topography. The proportion of high habitat suitability inside versus outside MPAs was higher when applying the historical predictions than the modern predictions, suggesting that different marine spatial planning optimums can be reached from either data sources. Moreover, differences in relative habitat suitability predictions between eras were consistent with the historical depletion of sperm whales from coastal regions, which were easily accessed and targeted by whalers, resulting in a modern distribution limited more to steep continental margins and remote oceanic ridges. The use of historical data can provide important new insights and, through cautious interpretation, inform conservation planning and policy, for example, by identifying refugee species and regions of anticipated population recovery.     

Effects of different management strategies on long-term trends of Australian threatened and near-threatened mammals

Monitoring is critical to assess management effectiveness, but broadscale systematic assessments of monitoring to evaluate and improve recovery efforts are lacking. We compiled 1808 time series from 71 threatened and near-threatened terrestrial and volant mammal species and subspecies in Australia (48% of all threatened mammal taxa) to compare relative trends of populations subject to different management strategies. We adapted the Living Planet Index to develop the Threatened Species Index for Australian Mammals and track aggregate trends for all sampled threatened mammal populations and for small (<35 g), medium (35–5500 g), and large mammals (>5500 g) from 2000 to 2017. Unmanaged populations (42 taxa) declined by 63% on average; unmanaged small mammals exhibited the greatest declines (96%). Populations of 17 taxa in havens (islands and fenced areas that excluded or eliminated introduced red foxes [Vulpes vulpes] and domestic cats [Felis catus]) increased by 680%. Outside havens, populations undergoing sustained predator baiting initially declined by 75% but subsequently increased to 47% of their abundance in 2000. At sites where predators were not excluded or baited but other actions (e.g., fire management, introduced herbivore control) occurred, populations of small and medium mammals declined faster, but large mammals declined more slowly, than unmanaged populations. Only 13% of taxa had data for both unmanaged and managed populations; index comparisons for this subset showed that taxa with populations increasing inside havens declined outside havens but taxa with populations subject to predator baiting outside havens declined more slowly than populations with no management and then increased, whereas unmanaged populations continued to decline. More comprehensive and improved monitoring (particularly encompassing poorly represented management actions and taxonomic groups like bats and small mammals) is required to understand whether and where management has worked. Improved implementation of management for threats other than predation is critical to recover Australia's threatened mammals.     

Fragmentation effects on an endangered species across a gradient from the interior to edge of its range

Understanding how habitat fragmentation affects individual species is complicated by challenges associated with quantifying species-specific habitat and spatial variability in fragmentation effects within a species’ range. We aggregated a 29-year breeding survey data set for the endangered marbled murrelet (Brachyramphus marmoratus) from >42,000 forest sites throughout the Pacific Northwest (Oregon, Washington, and northern California) of the United States. We built a species distribution model (SDM) in which occupied sites were linked with Landsat imagery to quantify murrelet-specific habitat and then used occupancy models to test the hypotheses that fragmentation negatively affects murrelet breeding distribution and that these effects are amplified with distance from the marine foraging habitat toward the edge of the species’ nesting range. Murrelet habitat declined in the Pacific Northwest by 20% since 1988, whereas the proportion of habitat comprising edges increased by 17%, indicating increased fragmentation. Furthermore, fragmentation of murrelet habitat at landscape scales (within 2 km of survey stations) negatively affected occupancy of potential breeding sites, and these effects were amplified near the range edge. On the coast, the odds of occupancy decreased by 37% (95% confidence interval [CI] –54 to 12) for each 10% increase in edge habitat (i.e., fragmentation), but at the range edge (88 km inland) these odds decreased by 99% (95% CI 98 to 99). Conversely, odds of murrelet occupancy increased by 31% (95% CI 14 to 52) for each 10% increase in local edge habitat (within 100 m of survey stations). Avoidance of fragmentation at broad scales but use of locally fragmented habitat with reduced quality may help explain the lack of murrelet population recovery. Further, our results emphasize that fragmentation effects can be nuanced, scale dependent, and geographically variable. Awareness of these nuances is critical for developing landscape-level conservation strategies for species experiencing broad-scale habitat loss and fragmentation.     

Factors associated with preemptive conservation under the U.S. Endangered Species Act

In recent decades, there has been an increasing emphasis on proactive efforts to conserve species being considered for listing under the U.S. Endangered Species Act (ESA) before they are listed (i.e., preemptive conservation). These efforts, which depend on voluntary actions by public and private land managers across the species’ range, aim to conserve species while avoiding regulatory costs associated with ESA listing. We collected data for a set of social, economic, environmental, and institutional factors that we hypothesized would influence voluntary decisions to promote or inhibit preemptive conservation of species under consideration for ESA listing. We used logistic regression to estimate the association of these factors with preemptive conservation outcomes based on data for a set of species that entered the ESA listing process and were either officially listed (n = 314) or preemptively conserved (n = 73) from 1996 to 2018. Factors significantly associated with precluded listing due to preemptive conservation included high baseline conservation status, low proportion of private land across the species’ range, small total range size, exposure to specific types of threats, and species’ range extending over several states. These results highlight strategies that can help improve conservation outcomes, such as allocating resources for imperiled species earlier in the listing process, addressing specific threats, and expanding incentives and coordination mechanisms for conservation on private lands.     

A critical review of the precautionary approach of the IUCN impact classification for non-native taxa

The International Union for the Conservation of Nature (IUCN) proposes the use of the Environmental Impact Classification for Alien Taxa to standardize the classification of introduced species (IS) based on their environmental impact. The IUCN invoked the precautionary principle (PP) via 2 rules: the impact assigned to a taxon must be the maximum recorded impact across different impact assessments, and when the main driver of environmental damage is unclear, it must be assumed to be caused by the IS. The validity of PP is conditioned on the degree of emergency that warrants urgent decisions and on the scientific evidence demonstrating the advantages of applying a preventive measure. The application of an impact classification system does not arise in the context of an emergency that requires management; it occurs before the decision-making phase. Thus, PP should not be used in early steps of the risk analysis process. The IUCN also did not provide enough scientific basis to justify the use of PP. Instead, the PP rules appear to be rooted primarily in the ethical value system underlying conservation science. Conservationists assign intrinsic value to native species by virtue of their roles and relationships within ecological and evolutionary systems and processes; thus, individuals introduced in new environments not only cease to have value because they are no longer part of that natural diversity and lack those links with the rest of the ecosystem, but they become a threat to what conservationists value most. The consequence of this belief is that all introduced taxa will have an impact at some level, suggesting that values justify the PP rules.     

Generation lengths of the world's birds and their implications for extinction risk

Birds have been comprehensively assessed on the International Union for Conservation of Nature (IUCN) Red List more times than any other taxonomic group. However, to date, generation lengths have not been systematically estimated to scale population trends when undertaking assessments, as required by the criteria of the IUCN Red List. We compiled information from major databases of published life-history and trait data for all birds and imputed missing life-history data as a function of species traits with generalized linear mixed models. Generation lengths were derived for all species, based on our modeled values of age at first breeding, maximum longevity, and annual adult survival. The resulting generation lengths varied from 1.42 to 27.87 years (median 2.99). Most species (61%) had generation lengths <3.33 years, meaning that the period of 3 generations—over which population declines are assessed under criterion A—was <10 years, which is the value used for IUCN Red List assessments of species with short generation times. For these species, our trait-informed estimates of generation length suggested that 10 years is a robust precautionary value for threat assessment. In other cases, however, for whole families, genera, or individual species, generation length had a substantial impact on their estimated extinction risk, resulting in higher extinction risk in long-lived species than in short-lived species. Although our approach effectively addressed data gaps, generation lengths for some species may have been underestimated due to a paucity of life-history data. Overall, our results will strengthen future extinction-risk assessments and augment key databases of avian life-history and trait data.