Population Viability Analysis with Species Occurrence Data from Museum Collections

Abstract: The most comprehensive data on many species come from scientific collections. Thus, we developed a method of population viability analysis (PVA) in which this type of occurrence data can be used. In contrast to classical PVA, our approach accounts for the inherent observation error in occurrence data and allows the estimation of the population parameters needed for viability analysis. We tested the sensitivity of the approach to spatial resolution of the data, length of the time series, sampling effort, and detection probability with simulated data and conducted PVAs for common, rare, and threatened species. We compared the results of these PVAs with results of standard method PVAs in which observation error is ignored. Our method provided realistic estimates of population growth terms and quasi‐extinction risk in cases in which the standard method without observation error could not. For low values of any of the sampling variables we tested, precision decreased, and in some cases biased estimates resulted. The results of our PVAs with the example species were consistent with information in the literature on these species. Our approach may facilitate PVA for a wide range of species of conservation concern for which demographic data are lacking but occurrence data are readily available.     

Global trends in research output by zoos and aquariums

Zoos and aquaria, often regarded as preservation-cum-entertainment enterprises, are also actors in the effort to curb the biodiversity crisis: raising awareness, supporting conservation, and conducting research. We assessed trends in zoo and aquaria research topics and study organisms over time worldwide. For the zoos and aquaria registered in the Species360's Zoological Information Management System and the World Association of Zoos and Aquariums, we compiled metadata on their research published in the peer-reviewed literature indexed in Scopus and carried out a keyword frequency analysis. The production of scientific papers by zoos increased at a much faster rate than the average accrual of scientific papers in the literature. Evolution of research themes ran parallel to that of biological sciences (e.g., development of molecular genetics or increased awareness about conservation). The focus of 48.5% of zoo-led research was on vertebrates, of which mammal research was 33.7%. Whether zoos are effectively contributing to conservation may still be debatable, but our results highlight their institutional efforts to increase knowledge about the species in their care.     

Application of multiple-population viability analysis to evaluate species recovery alternatives

Population viability analysis (PVA) is a powerful conservation tool, but it remains impractical for many species, particularly species with multiple, broadly distributed populations for which collecting suitable data can be challenging. A recently developed method of multiple-population viability analysis (MPVA), however, addresses many limitations of traditional PVA. We built on previous development of MPVA for Lahontan cutthroat trout (LCT) (Oncorhynchus clarkii henshawi), a species listed under the U.S. Endangered Species Act, that is distributed broadly across habitat fragments in the Great Basin (U.S.A.). We simulated potential management scenarios and assessed their effects on population sizes and extinction risks in 211 streams, where LCT exist or may be reintroduced. Conservation populations (those managed for recovery) tended to have lower extinction risks than nonconservation populations (mean = 19.8% vs. 52.7%), but not always. Active management or reprioritization may be warranted in some cases. Eliminating non-native trout had a strong positive effect on overall carrying capacities for LCT populations but often did not translate into lower extinction risks unless simulations also reduced associated stochasticity (to the mean for populations without non-native trout). Sixty fish or 5–10 fish/km was the minimum reintroduction number and density, respectively, that provided near-maximum reintroduction success. This modeling framework provided crucial insights and empirical justification for conservation planning and specific adaptive management actions for this threatened species. More broadly, MPVA is applicable to a wide range of species exhibiting geographic rarity and limited availability of abundance data and greatly extends the potential use of empirical PVA for conservation assessment and planning.     

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.     

Extinction risk of the endemic vascular flora of Kauai,Hawaii, based on IUCN assessments

The International Union for Conservation of Nature's Red List of Threatened Species (IUCN Red List) is the world's most comprehensive information source on the global conservation status of species. Governmental agencies and conservation organizations increasingly rely on IUCN Red List assessments to develop conservation policies and priorities. Funding agencies use the assessments as evaluation criteria, and researchers use meta-analysis of red-list data to address fundamental and applied conservation science questions. However, the circa 143,000 IUCN assessments represent a fraction of the world's biodiversity and are biased in regional and organismal coverage. These biases may affect conservation priorities, funding, and uses of these data to understand global patterns. Isolated oceanic islands are characterized by high endemicity, but the unique biodiversity of many islands is experiencing high extinction rates. The archipelago of Hawaii has one of the highest levels of endemism of any floristic region; 90% of its 1367 native vascular plant taxa are classified as endemic. We used the IUCN's assessment of the complete single-island endemic (SIE) vascular plant flora of Kauai, Hawaii, to assess the proportion and drivers of decline of threatened plants in an oceanic island setting. We compared the IUCN assessments with federal, state, and other local assessments of Kauai species or taxa of conservation concern. Finally, we conducted a preliminary assessment for all 1044 native vascular plants of Hawaii based on IUCN criterion B by estimating area of occupancy, extent of occurrence, and number of locations to determine whether the pattern found for the SIE vascular flora of Kauai is comparable to the native vascular flora of the Hawaiian Islands. We compared our results with patterns observed for assessments of other floras. According to IUCN, 256 SIE vascular plant taxa are threatened with extinction and 5% are already extinct. This is the highest extinction risk reported for any flora to date. The preliminary assessment of the native vascular flora of Hawaii showed that 72% (753 taxa) is threatened. The flora of Hawaii may be one of the world's most threatened; thus, increased and novel conservation measures in the state and on other remote oceanic islands are urgently needed.     

Difference in the net value of ecological services between natural and artificial forests in China

Land degradation is a global problem that seriously threatens human society. However, in China and elsewhere, ecological restoration still largely relies on a traditional approach that focuses only on ecological factors and ignores socioeconomic factors. To improve the effectiveness of ecological restoration and maximize its economic and ecological benefits, a more efficient approach is needed that provides support for policy development and land management and thereby promotes environmental conservation. We devised a framework for assessing the value of ecosystem services that remain after subtracting costs, such as the opportunity costs, costs of forest protection, and costs for the people who are affected by the program; that is, the net value of ecosystem services (NVES). To understand the difference between the value of a resource and the net value of the ecosystem service it provides, we used data on VES, timber sales, and afforestation costs from China's massive national afforestation programs to calculate the net value of forest ecosystem services in China. Accounting for the abovementioned costs revealed an NVES of ¥6.1 × 10¹² for forests in 2014, which was 35.9% less than the value calculated without accounting for costs. As a result, the NVES associated with afforestation was 55.9% less than the NVES of natural forests. In some regions, NVES was negative because of the huge costs of human-made plantations, high evapotranspiration rates (thus, high water opportunity costs), and low forest survival rates. To maximize the ecological benefits of conservation, it is necessary to account for as many costs as possible so that management decisions can be based on NVES, thereby helping managers choose projects that maximize both economic and ecological benefits.     

Speaking across boundaries to explore the potential for interdisciplinarity in ecosystem services knowledge production

Conservation is likely to be most successful if it draws on knowledge from across the natural and social sciences. The ecosystem services concept has been called a boundary object in that it facilitates development of such interdisciplinary knowledge because it offers a common platform for researchers, policy makers, and practitioners. However, a question that remains is to what extent the interdisciplinary knowledge needed is provided by disciplinary diversity within the field. We asked where is knowledge on ecosystem services produced, how interdisciplinary is this knowledge, and which disciplines facilitate the greatest disciplinary integration? We defined interdisciplinarity as the extent to which published research draws on knowledge that crosses disciplinary borders and used citations as a quantitative indicator of communication among disciplines, based on journal classification. We used disciplinary diversity, richness, and heterocitation as measures of interdisciplinarity and betweenness centrality as a measure of disciplinary integration. Our data set contained 22,153 publications on ecosystem services, published from 1983 to 2018. We found that ecosystem services research matured; average yearly output growth was 33.8%, more than the 8–9% growth in scientific output across all fields. Over time, the network clustering coefficient, measuring connectedness of individual disciplines, rose from 0.388 to 0.727, suggesting increased density in the network of citations. Researchers in the field published more articles (3566 in 2018 alone) across more disciplines (77 unique disciplines in 2018). However, this growth was not mirrored by an increase in the diversity (stable at 0.7–0.9) or richness (averaging 0.35 unique disciplines per citation) of citation patterns. Heterocitation scores, or out-of-group citations, for arts, humanities, social sciences, and law ranged from 56% to 64%, which was lower than we expected, although this may serve to protect the integrity of social science disciplines and attract broader engagement from within. Ultimately, a small number of productive disciplines are central to supporting disciplinary integration. However, opportunities exist for conservation practice to draw on a broader field of research, to realize the potential that the diverse body of knowledge of interdisciplinary work offers.     

Building a better baseline to estimate 160 years of avian population change and create historically informed conservation targets

Globally, anthropogenic land-cover change has been dramatic over the last few centuries and is frequently invoked as a major cause of wildlife population declines. Baseline data currently used to assess population trends, however, began well after major changes to the landscape. In the United States and Canada, breeding bird population trends are assessed by the North American Breeding Bird Survey, which began in the 1960s. Estimates of distribution and abundance prior to major habitat alteration would add historical perspective to contemporary trends and allow for historically based conservation targets. We used a hindcasting framework to estimate change in distribution and abundance of 7 bird species in the Willamette Valley, Oregon (United States). After reconciling classification schemes of current and 1850s reconstructed land cover, we used multiscale species distribution models and hierarchical distance sampling models to predict spatially explicit densities in the modern and historical landscapes. We estimated that since the 1850s, White-breasted Nuthatch (Sitta carolinensis) and Western Meadowlark (Sturnella neglecta) populations, 2 species sensitive to fragmentation of oak woodlands and grasslands, declined by 93% and 97%, respectively. Five other species we estimated nearly stable or increasing populations, despite steep regional declines since the 1960s. Based on these estimates, we developed historically based conservation targets for amount of habitat, population, and density for each species. Hindcasted reconstructions provide historical perspective for assessing contemporary trends and allow for historically based conservation targets that can inform current management.     

Prioritizing species conservation programs based on IUCN Green Status and estimates of cost-sharing potential

Over 1 million species around the world are at risk of extinction, and conservation organizations have to decide where to invest their limited resources. Cost-effectiveness can be increased by leveraging funding opportunities and increasing collaborative partnerships to achieve shared conservation goals. We devised a structured decision-making framework to prioritize species’ conservation programs based on a cost–benefit analysis that takes collaborative opportunities into account in an examination of national and global conservation return on investment. Conservation benefit is determined by modifying the novel International Union for the Conservation of Nature Green Status for Species to provide an efficient, high-level measure that is comparable among species, even with limited information and time constraints. We applied this prioritization approach to the Wilder Institute/Calgary Zoo, Canada, a nonprofit organization seeking to increase the number of species it assists with conservation translocations. We sought to identify and prioritize additional species’ programs for which conservation translocation expertise and actions could make the most impact. Estimating the likelihood of cost-sharing potential enabled total program cost to be distinguished from costs specific to the organization. Comparing a benefit-to-cost ratio on different geographic scales allowed decision makers to weigh alternative options for investing in new species’ programs in a transparent and effective manner. Our innovative analysis aligns with general conservation planning frameworks and can be adapted for any organization.     

A global ecological signal of extinction risk in terrestrial vertebrates

To determine the distribution and causes of extinction threat across functional groups of terrestrial vertebrates, we assembled an ecological trait data set for 18,016 species of terrestrial vertebrates and utilized phylogenetic comparative methods to test which categories of habitat association, mode of locomotion, and feeding mode best predicted extinction risk. We also examined the individual categories of the International Union for Conservation of Nature Red List extinction drivers (e.g., agriculture and logging) threatening each species and determined the greatest threats for each of the four terrestrial vertebrate groups. We then quantified the sum of extinction drivers threatening each species to provide a multistressor perspective on threat. Cave dwelling amphibians (p < 0.01), arboreal quadrupedal mammals (all of which are primates) (p < 0.01), aerial and scavenging birds (p < 0.01), and pedal (i.e., walking) squamates (p < 0.01) were all disproportionately threatened with extinction in comparison with the other assessed ecological traits. Across all threatened vertebrate species in the study, the most common risk factors were agriculture, threatening 4491 species, followed by logging, threatening 3187 species, and then invasive species and disease, threatening 2053 species. Species at higher risk of extinction were simultaneously at risk from a greater number of threat types. If left unabated, the disproportionate loss of species with certain functional traits and increasing anthropogenic pressures are likely to disrupt ecosystem functions globally. A shift in focus from species- to trait-centric conservation practices will allow for protection of at-risk functional diversity from regional to global scales.     

Bridging gaps in demographic analysis with phylogenetic imputation

Phylogenetically informed imputation methods have rarely been applied to estimate missing values in demographic data but may be a powerful tool for reconstructing vital rates of survival, maturation, and fecundity for species of conservation concern. Imputed vital rates could be used to parameterize demographic models to explore how populations respond when vital rates are perturbed. We used standardized vital rate estimates for 50 bird species to assess the use of phylogenetic imputation to fill gaps in demographic data. We calculated imputation accuracy for vital rates of focal species excluded from the data set either singly or in combination and with and without phylogeny, body mass, and life-history trait data. We used imputed vital rates to calculate demographic metrics, including generation time, to validate the use of imputation in demographic analyses. Covariance among vital rates and other trait data provided a strong basis to guide imputation of missing vital rates in birds, even in the absence of phylogenetic information. Mean NRMSE for null and phylogenetic models differed by <0.01 except when no vital rates were available or for vital rates with high phylogenetic signal (Pagel's λ > 0.8). In these cases, including body mass and life-history trait data compensated for lack of phylogenetic information: mean normalized root mean square error (NRMSE) for null and phylogenetic models differed by <0.01 for adult survival and <0.04 for maturation rate. Estimates of demographic metrics were sensitive to the accuracy of imputed vital rates. For example, mean error in generation time doubled in response to inaccurate estimates of maturation time. Accurate demographic data and metrics, such as generation time, are needed to inform conservation planning processes, for example through International Union for Conservation of Nature Red List assessments and population viability analysis. Imputed vital rates could be useful in this context but, as for any estimated model parameters, awareness of the sensitivities of demographic model outputs to the imputed vital rates is essential.     

Using expert knowledge to support Endangered Species Act decision-making for data-deficient species

Many questions relevant to conservation decision-making are characterized by extreme uncertainty due to lack of empirical data and complexity of the underlying ecologic processes, leading to a rapid increase in the use of structured protocols to elicit expert knowledge. Published ecologic applications often employ a modified Delphi method, where experts provide judgments anonymously and mathematical aggregation techniques are used to combine judgments. The Sheffield elicitation framework (SHELF) differs in its behavioral approach to synthesizing individual judgments into a fully specified probability distribution for an unknown quantity. We used the SHELF protocol remotely to assess extinction risk of three subterranean aquatic species that are being considered for listing under the U.S. Endangered Species Act. We provided experts an empirical threat assessment for each known locality over a video conference and recorded judgments on the probability of population persistence over four generations with online submission forms and R-shiny apps available through the SHELF package. Despite large uncertainty for all populations, there were key differences between species’ risk of extirpation based on spatial variation in dominant threats, local land use and management practices, and species’ microhabitat. The resulting probability distributions provided decision makers with a full picture of uncertainty that was consistent with the probabilistic nature of risk assessments. Discussion among experts during SHELF's behavioral aggregation stage clearly documented dominant threats (e.g., development, timber harvest, animal agriculture, and cave visitation) and their interactions with local cave geology and species’ habitat. Our virtual implementation of the SHELF protocol demonstrated the flexibility of the approach for conservation applications operating on budgets and time lines that can limit in-person meetings of geographically dispersed experts.     

Quantifying the impact of vegetation-based metrics on species persistence when choosing offsets for habitat destruction

Developers are often required by law to offset environmental impacts through targeted conservation actions. Most offset policies specify metrics for calculating offset requirements, usually by assessing vegetation condition. Despite widespread use, there is little evidence to support the effectiveness of vegetation-based metrics for ensuring biodiversity persistence. We compared long-term impacts of biodiversity offsetting based on area only; vegetation condition only; area × habitat suitability; and condition × habitat suitability in development and restoration simulations for the Hunter Region of New South Wales, Australia. We simulated development and subsequent offsetting through restoration within a virtual landscape, linking simulations to population viability models for 3 species. Habitat gains did not ensure species persistence. No net loss was achieved when performance of offsetting was assessed in terms of amount of habitat restored, but not when outcomes were assessed in terms of persistence. Maintenance of persistence occurred more often when impacts were avoided, giving further support to better enforce the avoidance stage of the mitigation hierarchy. When development affected areas of high habitat quality for species, persistence could not be guaranteed. Therefore, species must be more explicitly accounted for in offsets, rather than just vegetation or habitat alone. Declines due to a failure to account directly for species population dynamics and connectivity overshadowed the benefits delivered by producing large areas of high-quality habitat. Our modeling framework showed that the benefits delivered by offsets are species specific and that simple vegetation-based metrics can give misguided impressions on how well biodiversity offsets achieve no net loss.     

Importance of species translocations under rapid climate change

Species that cannot adapt or keep pace with a changing climate are likely to need human intervention to shift to more suitable climates. While hundreds of articles mention using translocation as a climate-change adaptation tool, in practice, assisted migration as a conservation action remains rare, especially for animals. This is likely due to concern over introducing species to places where they may become invasive. However, there are other barriers to consider, such as time-frame mismatch, sociopolitical, knowledge and uncertainty barriers to conservationists adopting assisted migration as a go-to strategy. We recommend the following to advance assisted migration as a conservation tool: attempt assisted migrations at small scales, translocate species with little invasion risk, adopt robust monitoring protocols that trigger an active response, and promote political and public support.     

Benefits of protected areas for nonbreeding waterbirds adjusting their distributions under climate warming

Climate warming is driving changes in species distributions and community composition. Many species have a so-called climatic debt, that is, shifts in range lag behind shifts in temperature isoclines. Inside protected areas (PAs), community changes in response to climate warming can be facilitated by greater colonization rates by warm-dwelling species, but also mitigated by lowering extirpation rates of cold-dwelling species. An evaluation of the relative importance of colonization-extirpation processes is important to inform conservation strategies that aim for both climate debt reduction and species conservation. We assessed the colonization-extirpation dynamics involved in community changes in response to climate inside and outside PAs. To do so, we used 25 years of occurrence data of nonbreeding waterbirds in the western Palearctic (97 species, 7071 sites, 39 countries, 1993–2017). We used a community temperature index (CTI) framework based on species thermal affinities to investigate species turnover induced by temperature increase. We determined whether thermal community adjustment was associated with colonization by warm-dwelling species or extirpation of cold-dwelling species by modeling change in standard deviation of the CTI (CTI_SD). Using linear mixed-effects models, we investigated whether communities in PAs had lower climatic debt and different patterns of community change than communities outside PAs. For CTI and CTI_SD combined, communities inside PAs had more species, higher colonization, lower extirpation, and lower climatic debt (16%) than communities outside PAs. Thus, our results suggest that PAs facilitate 2 independent processes that shape community dynamics and maintain biodiversity. The community adjustment was, however, not sufficiently fast to keep pace with the large temperature increases in the central and northeastern western Palearctic. Our results underline the potential of combining CTI and CTI_SD metrics to improve understanding of the colonization-extirpation patterns driven by climate warming.     

Improving inferences about private land conservation by accounting for incomplete reporting

Private lands provide key habitat for imperiled species and are core components of function protectected area networks; yet, their incorporation into national and regional conservation planning has been challenging. Identifying locations where private landowners are likely to participate in conservation initiatives can help avoid conflict and clarify trade-offs between ecological benefits and sociopolitical costs. Empirical, spatially explicit assessment of the factors associated with conservation on private land is an emerging tool for identifying future conservation opportunities. However, most data on private land conservation are voluntarily reported and incomplete, which complicates these assessments. We used a novel application of occupancy models to analyze the occurrence of conservation easements on private land. We compared multiple formulations of occupancy models with a logistic regression model to predict the locations of conservation easements based on a spatially explicit social–ecological systems framework. We combined a simulation experiment with a case study of easement data in Idaho and Montana (United States) to illustrate the utility of the occupancy framework for modeling conservation on private land. Occupancy models that explicitly accounted for variation in reporting produced estimates of predictors that were substantially less biased than estimates produced by logistic regression under all simulated conditions. Occupancy models produced estimates for the 6 predictors we evaluated in our case study that were larger in magnitude, but less certain than those produced by logistic regression. These results suggest that occupancy models result in qualitatively different inferences regarding the effects of predictors on conservation easement occurrence than logistic regression and highlight the importance of integrating variable and incomplete reporting of participation in empirical analysis of conservation initiatives. Failure to do so can lead to emphasizing the wrong social, institutional, and environmental factors that enable conservation and underestimating conservation opportunities in landscapes where social norms or institutional constraints inhibit reporting.     

Actual and Potential Use of Population Viability Analyses in Recovery of Plant Species Listed under the U.S. Endangered Species Act

Use of population viability analyses (PVAs) in endangered species recovery planning has been met with both support and criticism. Previous reviews promote use of PVA for setting scientifically based, measurable, and objective recovery criteria and recommend improvements to increase the framework's utility. However, others have questioned the value of PVA models for setting recovery criteria and assert that PVAs are more appropriate for understanding relative trade‐offs between alternative management actions. We reviewed 258 final recovery plans for 642 plants listed under the U.S. Endangered Species Act to determine the number of plans that used or recommended PVA in recovery planning. We also reviewed 223 publications that describe plant PVAs to assess how these models were designed and whether those designs reflected previous recommendations for improvement of PVAs. Twenty‐four percent of listed species had recovery plans that used or recommended PVA. In publications, the typical model was a matrix population model parameterized with ≤5 years of demographic data that did not consider stochasticity, genetics, density dependence, seed banks, vegetative reproduction, dormancy, threats, or management strategies. Population growth rates for different populations of the same species or for the same population at different points in time were often statistically different or varied by >10%. Therefore, PVAs parameterized with underlying vital rates that vary to this degree may not accurately predict recovery objectives across a species’ entire distribution or over longer time scales. We assert that PVA, although an important tool as part of an adaptive‐management program, can help to determine quantitative recovery criteria only if more long‐term data sets that capture spatiotemporal variability in vital rates become available. Lacking this, there is a strong need for viable and comprehensive methods for determining quantitative, science‐based recovery criteria for endangered species with minimal data availability. Uso Actual y Potencial del Análisis de Viabilidad Poblacional para la Recuperación de Especies de Plantas Enlistadas en el Acta de Especies En Peligro de E.U.A     

Using ensemble modeling to predict the impacts of assisted migration on recipient ecosystems

Assisted migration is a controversial conservation measure that aims to protect threatened species by moving part of their population outside its natural range. Although this could save species from extinction, it also introduces a range of risks. The magnitude of the threat to recipient ecosystems has not been investigated quantitatively, despite being the most common criticism leveled at the action. We used an ensemble modeling framework to estimate the risks of assisted migration to existing species within ecosystems. With this approach, we calculated the consequences of an assisted migration project across a very large combination of translocated species and recipient ecosystems. We predicted the probability of a successful assisted migration and the number of local extinctions would result from establishment of the translocated species. Using an ensemble of simulated 15-species recipient ecosystems, we estimated that translocated species will successfully establish in 83% of cases if introduced to stable, high-quality habitats. However, assisted migration projects were estimated to cause an average of 0.6 extinctions and 5% of successful translocations triggered 4 or more local extinctions. Quantifying the impacts to species within recipient ecosystems is critical to help managers weigh the benefits and negative consequences of assisted migration.