Correction: Public preferences for ecological indicators used in Everglades restoration.

[This corrects the article DOI: 10.1371/journal.pone.0234051.].

Public preferences for ecological indicators used in Everglades restoration.

The Everglades is one of the largest wetland ecosystems in the world covering almost 18,000 square miles from central Florida southward to Florida Bay. Over the 20th century, efforts to drain the Everglades for agriculture and development severely damaged the ecosystem so that today roughly 50% of the historic flow of water through the Everglades has been diverted elsewhere. In an attempt to restore the Everglades, the U.S. Congress authorized the Comprehensive Everglades Restoration Plan (CERP) in 2000, expected to cost over $16 billion and to take several decades to complete. We used the results from a stated preference choice experiment (SPCE) survey of Florida households to estimate the willingness to pay for several ecological attributes related to CERP performance indicators likely to be impacted by Everglades restoration. We also used a latent class model (LCM) to explore preference heterogeneity among respondents. On average, survey respondents were willing to pay for improvements in all of the attributes included in the survey, namely increased populations of wading birds, American alligators, endangered snail kites, and spotted seatrout, and reduced polluted discharges from Lake Okeechobee to the Caloosahatchee and St. Lucie rivers. Willingness to pay was highest for reduced polluted discharges from Lake Okeechobee.

Ecosystem service flows from a migratory species: Spatial subsidies of the northern pintail.

Migratory species provide important benefits to society, but their cross-border conservation poses serious challenges. By quantifying the economic value of ecosystem services (ESs) provided across a species' range and ecological data on a species' habitat dependence, we estimate spatial subsidies-how different regions support ESs provided by a species across its range. We illustrate this method for migratory northern pintail ducks in North America. Pintails support over $101 million USD annually in recreational hunting and viewing and subsistence hunting in the U.S. and Canada. Pintail breeding regions provide nearly $30 million in subsidies to wintering regions, with the "Prairie Pothole" region supplying over $24 million in annual benefits to other regions. This information can be used to inform conservation funding allocation among migratory regions and nations on which the pintail depends. We thus illustrate a transferrable method to quantify migratory species-derived ESs and provide information to aid in their transboundary conservation.

Willingness to Pay for Conservation of Transborder Migratory Species: A Case Study of the Mexican Free-Tailed Bat in the United States and Mexico.

We estimated U.S. and Mexican citizens' willingness to pay (WTP) for protecting habitat for a transborder migratory species, the Mexican free-tailed bat (Tadarida brasiliensis mexicana), using the contingent valuation method. Few contingent valuation surveys have evaluated whether households in one country would pay to protect habitat in another country. This study addresses that gap. In our study, Mexican respondents were asked about their WTP for conservation of Mexican free-tailed bat habitat in Mexico and in the United States. Similarly, U.S. respondents were asked about their WTP for conservation in the United States and in Mexico. U.S. households would pay $30 annually to protect habitat in the United States and $24 annually to protect habitat in Mexico. Mexican households would pay $8 annually to protect habitat in Mexico and $5 annually to protect habitat in the United States. In both countries, these WTP amounts rose significantly for increasing the size of the bat population rather than simply stabilizing the current bat population. The ratio of Mexican household WTP relative to U.S. household WTP is nearly identical to that of Mexican household income relative to U.S. household income. This suggests that the perceived economic benefits received from the bats is similar in Mexico and the United States, and that scaling WTP by relative income in international benefit transfer may be plausible.

A general modeling framework for describing spatially structured population dynamics.

Variation in movement across time and space fundamentally shapes the abundance and distribution of populations. Although a variety of approaches model structured population dynamics, they are limited to specific types of spatially structured populations and lack a unifying framework. Here, we propose a unified network-based framework sufficiently novel in its flexibility to capture a wide variety of spatiotemporal processes including metapopulations and a range of migratory patterns. It can accommodate different kinds of age structures, forms of population growth, dispersal, nomadism and migration, and alternative life-history strategies. Our objective was to link three general elements common to all spatially structured populations (space, time and movement) under a single mathematical framework. To do this, we adopt a network modeling approach. The spatial structure of a population is represented by a weighted and directed network. Each node and each edge has a set of attributes which vary through time. The dynamics of our network-based population is modeled with discrete time steps. Using both theoretical and real-world examples, we show how common elements recur across species with disparate movement strategies and how they can be combined under a unified mathematical framework. We illustrate how metapopulations, various migratory patterns, and nomadism can be represented with this modeling approach. We also apply our network-based framework to four organisms spanning a wide range of life histories, movement patterns, and carrying capacities. General computer code to implement our framework is provided, which can be applied to almost any spatially structured population. This framework contributes to our theoretical understanding of population dynamics and has practical management applications, including understanding the impact of perturbations on population size, distribution, and movement patterns. By working within a common framework, there is less chance that comparative analyses are colored by model details rather than general principles.

Quantitative tools for implementing the new definition of significant portion of the range in the U.S. Endangered Species Act.

In 2014, the Fish and Wildlife Service (FWS) and National Marine Fisheries Service announced a new policy interpretation for the U.S. Endangered Species Act (ESA). According to the act, a species must be listed as threatened or endangered if it is determined to be threatened or endangered in a significant portion of its range (SPR). The 2014 policy seeks to provide consistency by establishing that a portion of the range should be considered significant if the associated individuals' "removal would cause the entire species to become endangered or threatened." We reviewed 20 quantitative techniques used to assess whether a portion of a species' range is significant according to the new guidance. Our assessments are based on the 3R criteria-redundancy (i.e., buffering from catastrophe), resiliency (i.e., ability to withstand stochasticity), and representation (i.e., ability to evolve)-that the FWS uses to determine if a species merits listing. We identified data needs for each quantitative technique and considered which methods could be implemented given the data limitations typical of rare species. We also identified proxies for the 3Rs that may be used with limited data. To assess potential data availability, we evaluated 7 example species by accessing data in their species status assessments, which document all the information used during a listing decision. In all species, an SPR could be evaluated with at least one metric for each of the 3Rs robustly or with substantial assumptions. Resiliency assessments appeared most constrained by limited data, and many species lacked information on connectivity between subpopulations, genetic variation, and spatial variability in vital rates. These data gaps will likely make SPR assessments for species with complex life histories or that cross national boundaries difficult. Although we reviewed techniques for the ESA, other countries require identification of significant areas and could benefit from this research.

Recreation economics to inform migratory species conservation: Case study of the northern pintail.

Quantification of the economic value provided by migratory species can aid in targeting management efforts and funding to locations yielding the greatest benefits to society and species conservation. Here we illustrate a key step in this process by estimating hunting and birding values of the northern pintail (Anas acuta) within primary breeding and wintering habitats used during the species' annual migratory cycle in North America. We used published information on user expenditures and net economic values (consumer surplus) for recreational viewing and hunting to determine the economic value of pintail-based recreation in three primary breeding areas and two primary wintering areas. Summed expenditures and consumer surplus for northern pintail viewing were annually valued at $70M, and annual sport hunting totaled $31M (2014 USD). Expenditures for viewing ($42M) were more than twice as high than those for hunting ($18M). Estimates of consumer surplus, defined as the amount consumers are willing to pay above their current expenditures, were $15M greater for viewing ($28M) than for hunting ($13M). We discovered substantial annual consumer surplus ($41M) available for pintail conservation from birders and hunters. We also found spatial differences in economic value among the primary regions used by pintails, with viewing generally valued more in breeding regions than in wintering regions and the reverse being true for hunting. The economic value of pintail-based recreation in the Western wintering region ($26M) exceeded that in any other region by at least a factor of three. Our approach of developing regionally explicit economic values can be extended to other taxonomic groups, and is particularly suitable for migratory game birds because of the availability of large amounts of data. When combined with habitat-linked population models, regionally explicit values could inform development of more effective conservation finance and policy mechanisms to enhance environmental management and societal benefits across the geographically dispersed areas used by migratory species.

Monarch butterfly population decline in North America: identifying the threatening processes.

The monarch butterfly (Danaus plexippus) population in North America has sharply declined over the last two decades. Despite rising concern over the monarch butterfly's status, no comprehensive study of the factors driving this decline has been conducted. Using partial least-squares regressions and time-series analysis, we investigated climatic and habitat-related factors influencing monarch population size from 1993 to 2014. Potential threats included climatic factors, habitat loss (milkweed and overwinter forest), disease and agricultural insecticide use (neonicotinoids). While climatic factors, principally breeding season temperature, were important determinants of annual variation in abundance, our results indicated strong negative relationships between population size and habitat loss variables, principally glyphosate use, but also weaker negative effects from the loss of overwinter forest and breeding season use of neonicotinoids. Further declines in population size because of glyphosate application are not expected. Thus, if remaining threats to habitat are mitigated we expect climate-induced stochastic variation of the eastern migratory population of monarch butterfly around a relatively stationary population size.

Density estimates of monarch butterflies overwintering in central Mexico.

Given the rapid population decline and recent petition for listing of the monarch butterfly (Danaus plexippus L.) under the Endangered Species Act, an accurate estimate of the Eastern, migratory population size is needed. Because of difficulty in counting individual monarchs, the number of hectares occupied by monarchs in the overwintering area is commonly used as a proxy for population size, which is then multiplied by the density of individuals per hectare to estimate population size. There is, however, considerable variation in published estimates of overwintering density, ranging from 6.9-60.9 million ha-1. We develop a probability distribution for overwinter density of monarch butterflies from six published density estimates. The mean density among the mixture of the six published estimates was ∼27.9 million butterflies ha-1 (95% CI [2.4-80.7] million ha-1); the mixture distribution is approximately log-normal, and as such is better represented by the median (21.1 million butterflies ha-1). Based upon assumptions regarding the number of milkweed needed to support monarchs, the amount of milkweed (Asclepias spp.) lost (0.86 billion stems) in the northern US plus the amount of milkweed remaining (1.34 billion stems), we estimate >1.8 billion stems is needed to return monarchs to an average population size of 6 ha. Considerable uncertainty exists in this required amount of milkweed because of the considerable uncertainty occurring in overwinter density estimates. Nevertheless, the estimate is on the same order as other published estimates. The studies included in our synthesis differ substantially by year, location, method, and measures of precision. A better understanding of the factors influencing overwintering density across space and time would be valuable for increasing the precision of conservation recommendations.

Quasi-extinction risk and population targets for the Eastern, migratory population of monarch butterflies (Danaus plexippus).

The Eastern, migratory population of monarch butterflies (Danaus plexippus), an iconic North American insect, has declined by ~80% over the last decade. The monarch's multi-generational migration between overwintering grounds in central Mexico and the summer breeding grounds in the northern U.S. and southern Canada is celebrated in all three countries and creates shared management responsibilities across North America. Here we present a novel Bayesian multivariate auto-regressive state-space model to assess quasi-extinction risk and aid in the establishment of a target population size for monarch conservation planning. We find that, given a range of plausible quasi-extinction thresholds, the population has a substantial probability of quasi-extinction, from 11-57% over 20 years, although uncertainty in these estimates is large. Exceptionally high population stochasticity, declining numbers, and a small current population size act in concert to drive this risk. An approximately 5-fold increase of the monarch population size (relative to the winter of 2014-15) is necessary to halve the current risk of quasi-extinction across all thresholds considered. Conserving the monarch migration thus requires active management to reverse population declines, and the establishment of an ambitious target population size goal to buffer against future environmentally driven variability.

Scaling up the diversity-resilience relationship with trait databases and remote sensing data: the recovery of productivity after wildfire.

Understanding the mechanisms underlying ecosystem resilience - why some systems have an irreversible response to disturbances while others recover - is critical for conserving biodiversity and ecosystem function in the face of global change. Despite the widespread acceptance of a positive relationship between biodiversity and resilience, empirical evidence for this relationship remains fairly limited in scope and localized in scale. Assessing resilience at the large landscape and regional scales most relevant to land management and conservation practices has been limited by the ability to measure both diversity and resilience over large spatial scales. Here, we combined tools used in large-scale studies of biodiversity (remote sensing and trait databases) with theoretical advances developed from small-scale experiments to ask whether the functional diversity within a range of woodland and forest ecosystems influences the recovery of productivity after wildfires across the four-corner region of the United States. We additionally asked how environmental variation (topography, macroclimate) across this geographic region influences such resilience, either directly or indirectly via changes in functional diversity. Using path analysis, we found that functional diversity in regeneration traits (fire tolerance, fire resistance, resprout ability) was a stronger predictor of the recovery of productivity after wildfire than the functional diversity of seed mass or species richness. Moreover, slope, elevation, and aspect either directly or indirectly influenced the recovery of productivity, likely via their effect on microclimate, while macroclimate had no direct or indirect effects. Our study provides some of the first direct empirical evidence for functional diversity increasing resilience at large spatial scales. Our approach highlights the power of combining theory based on local-scale studies with tools used in studies at large spatial scales and trait databases to understand pressing environmental issues.

The face of conservation responding to a dynamically changing world.

In its 40-year history, the science of conservation has faced unprecedented challenges in terms of environmental damage and rapid global change, and environmental problems are only increasing as greater demands are placed on limited natural resources. Conservation science has been adapting to keep pace with these changes. Here, we highlight contemporary and emerging trends and innovations in conservation science that we believe represent the most effective responses to biodiversity threats. We focus on specific areas where conservation science has had to adjust its approach to address emerging threats to biodiversity, including habitat destruction and degradation, climate change, declining populations and invasive species. We also document changes in attitudes, norms and practices among conservation scientists. A key component to success is engaging and maintaining public support for conservation, which can be facilitated through the use of technology. These recent trends in conservation and management are innovative and will assist in optimizing conservation strategies, increasing our leverage with the general public and tackling our current environmental challenges.

Market forces and technological substitutes cause fluctuations in the value of bat pest-control services for cotton.

Critics of the market-based, ecosystem services approach to biodiversity conservation worry that volatile market conditions and technological substitutes will diminish the value of ecosystem services and obviate the "economic benefits" arguments for conservation. To explore the effects of market forces and substitutes on service values, we assessed how the value of the pest-control services provided by Mexican free-tailed bats (Tadarida brasiliensis mexicana) to cotton production in the southwestern U.S. has changed over time. We calculated service values each year from 1990 through 2008 by estimating the value of avoided crop damage and the reduced social and private costs of insecticide use in the presence of bats. Over this period, the ecosystem service value declined by 79% ($19.09 million U.S. dollars) due to the introduction and widespread adoption of Bt (Bacillus thuringiensis) cotton transgenically modified to express its own pesticide, falling global cotton prices and the reduction in the number of hectares in the U.S. planted with cotton. Our results demonstrate that fluctuations in market conditions can cause temporal variation in ecosystem service values even when ecosystem function--in this case bat population numbers--is held constant. Evidence is accumulating, however, of the evolution of pest resistance to Bt cotton, suggesting that the value of bat pest-control services may increase again. This gives rise to an economic option value argument for conserving Mexican free-tailed bat populations. We anticipate that these results will spur discussion about the role of ecosystem services in biodiversity conservation in general, and bat conservation in particular.

Tropical warming and the dynamics of endangered primates.

Many primate species are severely threatened, but little is known about the effects of global warming and the associated intensification of El Niño events on primate populations. Here, we document the influences of the El Niño southern oscillation (ENSO) and hemispheric climatic variability on the population dynamics of four genera of ateline (neotropical, large-bodied) primates. All ateline genera experienced either an immediate or a lagged negative effect of El Niño events. ENSO events were also found to influence primate resource levels through neotropical arboreal phenology. Furthermore, frugivorous primates showed a high degree of interspecific population synchrony over large scales across Central and South America attributable to the recent trends in large-scale climate. These results highlight the role of large-scale climatic variation and trends in ateline primate population dynamics, and emphasize that global warming could pose additional threats to the persistence of multiple species of endangered primates.