Mammals, wildlife trade, and the next global pandemic.

Most new infectious diseases emerge when pathogens transfer from animals to humans.1,2 The suspected origin of the COVID pandemic in a wildlife wet market has resurfaced debates on the role of wildlife trade as a potential source of emerging zoonotic diseases.3-5 Yet there are no studies quantitatively assessing zoonotic disease risk associated with wildlife trade. Combining data on mammal species hosting zoonotic viruses and mammals known to be in current and future wildlife trade,6 we found that one-quarter (26.5%) of the mammals in wildlife trade harbor 75% of known zoonotic viruses, a level much higher than domesticated and non-traded mammals. The traded mammals also harbor distinct compositions of zoonotic viruses and different host reservoirs from non-traded and domesticated mammals. Furthermore, we highlight that primates, ungulates, carnivores, and bats represent significant zoonotic disease risks as they host 132 (58%) of 226 known zoonotic viruses in present wildlife trade, whereas species of bats, rodents, and marsupials represent significant zoonotic disease risks in future wildlife trade. Thus, the risk of carrying zoonotic diseases is not equal for all mammal species in wildlife trade. Overall, our findings strengthen the evidence that wildlife trade and zoonotic disease risks are strongly associated, and that mitigation measures should prioritize species with the highest risk of carrying zoonotic viruses. Curbing the sales of wildlife products and developing principles that support the sustainable and healthy trade of wildlife could be cost-effective investments given the potential risk and consequences of zoonotic outbreaks.

Local conditions and policy design determine whether ecological compensation can achieve No Net Loss goals.

Many nations use ecological compensation policies to address negative impacts of development projects and achieve No Net Loss (NNL) of biodiversity and ecosystem services. Yet, failures are widely reported. We use spatial simulation models to quantify potential net impacts of alternative compensation policies on biodiversity (indicated by native vegetation) and two ecosystem services (carbon storage, sediment retention) across four case studies (in Australia, Brazil, Indonesia, Mozambique). No policy achieves NNL of biodiversity in any case study. Two factors limit their potential success: the land available for compensation (existing vegetation to protect or cleared land to restore), and expected counterfactual biodiversity losses (unregulated vegetation clearing). Compensation also fails to slow regional biodiversity declines because policies regulate only a subset of sectors, and expanding policy scope requires more land than is available for compensation activities. Avoidance of impacts remains essential in achieving NNL goals, particularly once opportunities for compensation are exhausted.

Unconventional oil and gas spills: Materials, volumes, and risks to surface waters in four states of the U.S.

Extraction of oil and gas from unconventional sources, such as shale, has dramatically increased over the past ten years, raising the potential for spills or releases of chemicals, waste materials, and oil and gas. We analyzed spill data associated with unconventional wells from Colorado, New Mexico, North Dakota and Pennsylvania from 2005 to 2014, where we defined unconventional wells as horizontally drilled into an unconventional formation. We identified materials spilled by state and for each material we summarized frequency, volumes and spill rates. We evaluated the environmental risk of spills by calculating distance to the nearest stream and compared these distances to existing setback regulations. Finally, we summarized relative importance to drinking water in watersheds where spills occurred. Across all four states, we identified 21,300 unconventional wells and 6622 reported spills. The number of horizontal well bores increased sharply beginning in the late 2000s; spill rates also increased for all states except PA where the rate initially increased, reached a maximum in 2009 and then decreased. Wastewater, crude oil, drilling waste, and hydraulic fracturing fluid were the materials most often spilled; spilled volumes of these materials largely ranged from 100 to 10,000L. Across all states, the average distance of spills to a stream was highest in New Mexico (1379m), followed by Colorado (747m), North Dakota (598m) and then Pennsylvania (268m), and 7.0, 13.3, and 20.4% of spills occurred within existing surface water setback regulations of 30.5, 61.0, and 91.4m, respectively. Pennsylvania spills occurred in watersheds with a higher relative importance to drinking water than the other three states. Results from this study can inform risk assessments by providing improved input parameters on volume and rates of materials spilled, and guide regulations and the management policy of spills.

Shale gas, wind and water: assessing the potential cumulative impacts of energy development on ecosystem services within the Marcellus play.

Global demand for energy has increased by more than 50 percent in the last half-century, and a similar increase is projected by 2030. This demand will increasingly be met with alternative and unconventional energy sources. Development of these resources causes disturbances that strongly impact terrestrial and freshwater ecosystems. The Marcellus Shale gas play covers more than 160,934 km(2) in an area that provides drinking water for over 22 million people in several of the largest metropolitan areas in the United States (e.g. New York City, Washington DC, Philadelphia & Pittsburgh). Here we created probability surfaces representing development potential of wind and shale gas for portions of six states in the Central Appalachians. We used these predictions and published projections to model future energy build-out scenarios to quantify future potential impacts on surface drinking water. Our analysis predicts up to 106,004 new wells and 10,798 new wind turbines resulting up to 535,023 ha of impervious surface (3% of the study area) and upwards of 447,134 ha of impacted forest (2% of the study area). In light of this new energy future, mitigating the impacts of energy development will be one of the major challenges in the coming decades.

Win-win for wind and wildlife: a vision to facilitate sustainable development.

Wind energy offers the potential to reduce carbon emissions while increasing energy independence and bolstering economic development. However, wind energy has a larger land footprint per Gigawatt (GW) than most other forms of energy production, making appropriate siting and mitigation particularly important. Species that require large unfragmented habitats and those known to avoid vertical structures are particularly at risk from wind development. Developing energy on disturbed lands rather than placing new developments within large and intact habitats would reduce cumulative impacts to wildlife. The U.S. Department of Energy estimates that it will take 241 GW of terrestrial based wind development on approximately 5 million hectares to reach 20% electricity production for the U.S. by 2030. We estimate there are ∼7,700 GW of potential wind energy available across the U.S., with ∼3,500 GW on disturbed lands. In addition, a disturbance-focused development strategy would avert the development of ∼2.3 million hectares of undisturbed lands while generating the same amount of energy as development based solely on maximizing wind potential. Wind subsidies targeted at favoring low-impact developments and creating avoidance and mitigation requirements that raise the costs for projects impacting sensitive lands could improve public value for both wind energy and biodiversity conservation.

Global stressors and the global decline of amphibians: tipping the stress immunocompetency axis.

There is a widespread consensus that the earth is experiencing a mass extinction event and at the forefront are amphibians, the most threatened of all vertebrate taxa. A recent assessment found that nearly one-third (32%, 1,856 species) of the world's amphibian species are threatened. Amphibians have existed on the earth for over 300 million years, yet in just the last two decades there have been an alarming number of extinctions, nearly 168 species are believed to have gone extinct and at least 2,469 (43%) more have populations that are declining. Infectious diseases have been recognized as one major cause of worldwide amphibian population declines. This could be the result of the appearance of novel pathogens, or it could be that exposure to environmental stressors is increasing the susceptibility of amphibians to opportunistic pathogens. Here I review the potential effects of stressors on disease susceptibility in amphibians and relate this to disease emergence in human and other wildlife populations. I will present a series of case studies that illustrate the role of stress in disease outbreaks that have resulted in amphibian declines. First, I will examine how elevated sea-surface temperatures in the tropical Pacific since the mid-1970s have affected climate over much of the world and could be setting the stage for pathogen-mediated amphibian declines in many regions. Finally, I will discuss how the apparently rapid increase in the prevalence of amphibian limb deformities is linked to the synergistic effects of trematode infection and exposure to chemical contaminants.

Variation in the hormonal stress response among larvae of three amphibian species.

In a series of studies, we examined how larval corticosterone treatment for several species of amphibians can impact fitness parameters both during exposure and after metamorphosis. We completed confinement stress series on larvae of three species in natural/semi-natural conditions: wood frogs (Rana sylvatica), Jefferson salamanders (Ambystoma jeffersonianum), and Eastern spadefoot toads (Scaphiopus holbrooki). Two of the species had a typical vertebrate response of increasing corticosterone with confinement. However, Eastern spadefoot toads, which have a very short developmental period before metamorphosis, did not show any increase in corticosterone in response to confinement. In a second study, we treated the three species with a low and a high concentration of corticosterone (0.001 and 0.01 µM dissolved in tank water) in the laboratory and examined effects on growth. Although we were successful in raising baseline corticosterone levels with our high corticosterone concentrations, this did not translate into changes in mean larval growth for any of the three species. The larval treatments also did not appear to translate into differences in the juvenile response to confinement stress after metamorphosis. Although juvenile wood frogs did respond to confinement with increasing corticosterone, there was no variation based on larval treatment. As with the larval responses, the juvenile Eastern spadefoot toads did not have a hormonal response to confinement. In summary, while our larval corticosterone exposures did elevate baseline corticosterone levels, we did not see effects of exposure on growth or any latent effects of larval exposure on juvenile responses to confinement.

Policy development for biodiversity offsets: a review of offset frameworks.

Biodiversity offsets seek to compensate for residual environmental impacts of planned developments after appropriate steps have been taken to avoid, minimize or restore impacts on site. Offsets are emerging as an increasingly employed mechanism for achieving net environmental benefits, with offset policies being advanced in a wide range of countries (i.e., United States, Australia, Brazil, Colombia, and South Africa). To support policy development for biodiversity offsets, we review a set of major offset policy frameworks-US wetlands mitigation, US conservation banking, EU Natura 2000, Australian offset policies in New South Wales, Victoria, and Western Australia, and Brazilian industrial and forest offsets. We compare how the frameworks define offset policy goals, approach the mitigation process, and address six key issues for implementing offsets: (1) equivalence of project impacts with offset gains; (2) location of the offset relative to the impact site; (3) "additionality" (a new contribution to conservation) and acceptable types of offsets; (4) timing of project impacts versus offset benefits; (5) offset duration and compliance; and (6) "currency" and mitigation replacement ratios. We find substantial policy commonalities that may serve as a sound basis for future development of biodiversity offsets policy. We also identify issues requiring further policy guidance, including how best to: (1) ensure conformance with the mitigation hierarchy; (2) identify the most environmentally preferable offsets within a landscape context; and (3) determine appropriate mitigation replacement ratios.

Mapping oil and gas development potential in the US Intermountain West and estimating impacts to species.

BACKGROUND: Many studies have quantified the indirect effect of hydrocarbon-based economies on climate change and biodiversity, concluding that a significant proportion of species will be threatened with extinction. However, few studies have measured the direct effect of new energy production infrastructure on species persistence. METHODOLOGY/PRINCIPAL FINDINGS: We propose a systematic way to forecast patterns of future energy development and calculate impacts to species using spatially-explicit predictive modeling techniques to estimate oil and gas potential and create development build-out scenarios by seeding the landscape with oil and gas wells based on underlying potential. We illustrate our approach for the greater sage-grouse (Centrocercus urophasianus) in the western US and translate the build-out scenarios into estimated impacts on sage-grouse. We project that future oil and gas development will cause a 7-19 percent decline from 2007 sage-grouse lek population counts and impact 3.7 million ha of sagebrush shrublands and 1.1 million ha of grasslands in the study area. CONCLUSIONS/SIGNIFICANCE: Maps of where oil and gas development is anticipated in the US Intermountain West can be used by decision-makers intent on minimizing impacts to sage-grouse. This analysis also provides a general framework for using predictive models and build-out scenarios to anticipate impacts to species. These predictive models and build-out scenarios allow tradeoffs to be considered between species conservation and energy development prior to implementation.

Epidermal 'alarm substance' cells of fishes maintained by non-alarm functions: possible defence against pathogens, parasites and UVB radiation.

Many fishes possess specialized epidermal cells that are ruptured by the teeth of predators, thus reliably indicating the presence of an actively foraging predator. Understanding the evolution of these cells has intrigued evolutionary ecologists because the release of these alarm chemicals is not voluntary. Here, we show that predation pressure does not influence alarm cell production in fishes. Alarm cell production is stimulated by exposure to skin-penetrating pathogens (water moulds: Saprolegnia ferax and Saprolegnia parasitica), skin-penetrating parasites (larval trematodes: Teleorchis sp. and Uvulifer sp.) and correlated with exposure to UV radiation. Suppression of the immune system with environmentally relevant levels of Cd inhibits alarm cell production of fishes challenged with Saprolegnia. These data are the first evidence that alarm substance cells have an immune function against ubiquitous environmental challenges to epidermal integrity. Our results indicate that these specialized cells arose and are maintained by natural selection owing to selfish benefits unrelated to predator-prey interactions. Cell contents released when these cells are damaged in predator attacks have secondarily acquired an ecological role as alarm cues because selection favours receivers to detect and respond adaptively to public information about predation.

Searching for the physiological mechanism of density dependence: does corticosterone regulate tadpole responses to density?

Density-dependent population regulation is important in many natural populations, and in those populations, high population density is a likely stressor. In amphibians, previous laboratory studies with tadpoles suggest that corticosterone, the main glucocorticoid stress hormone, is one of the key regulators of density-dependent growth. To test this relationship in natural settings, we manipulated wood frog (Rana sylvatica) tadpole density at three levels in outdoor mesocosms and used a capture stress protocol to examine the hormonal stress response. In addition, we used the same capture protocol in six natural ponds (three high density and three low density). In the mesocosms, there was an increase in corticosterone levels in tadpoles following 1 h of confinement at weeks 1, 2, and 5. However, while tadpoles maintained at higher densities were smaller after metamorphosis, density did not alter mean levels of corticosterone obtained during confinement, and baseline levels of corticosterone did not differ between the densities. Similarly, in natural ponds, density did not correlate with baseline corticosterone or mean corticosterone levels obtained during confinement. We suggest that the physiological response to density may vary across the range of natural densities and that the role of corticosterone may be limited to periods of extreme high density, such as during pond-drying events.

Conservation easements: biodiversity protection and private use.

Conservation easements are one of the primary tools for conserving biodiversity on private land. Despite their increasing use, little quantitative data are available on what species and habitats conservation easements aim to protect, how much structural development they allow, or what types of land use they commonly permit. To address these knowledge gaps, we surveyed staff responsible for 119 conservation easements established by the largest nonprofit easement holder, The Nature Conservancy, between 1985 and 2004. Most easements (80%) aimed to provide core habitat to protect species or communities on-site, and nearly all were designed to reduce development. Conservation easements also allowed for a wide range of private uses, which may result in additional fragmentation and habitat disturbance. Some residential or commercial use, new structures, or subdivision of the property were permitted on 85% of sampled conservation easements. Over half (56%) allowed some additional buildings, of which 60% restricted structure size or building area. Working landscape easements with ranching, forestry, or farming made up nearly half (46%) of the easement properties sampled and were more likely than easements without these uses to be designated as buffers to enhance biodiversity in the surrounding area. Our results demonstrate the need for clear restrictions on building and subdivision in easements, research on the compatibility of private uses on easement land, and greater public understanding of the trade-offs implicit in the use of conservation easements for biodiversity conservation.

Survivorship patterns of larval amphibians exposed to low concentrations of atrazine.

Amphibians can be exposed to contaminants in nature by many routes, but perhaps the most likely route is agricultural runoff in amphibian breeding sites. This runoff results in high-level pulses of pesticides. For example, atrazine, the most widely used pesticide in the United States, can be present at several parts per million in agricultural runoff. However, pesticide levels are likely to remain in the environment at low levels for longer periods. Nevertheless, most studies designed to examine the impacts of contaminants are limited to short-term (approximately 4 days) tests conducted at relatively high concentrations. To investigate longer-term (approximately 30 days) exposure of amphibians to low pesticide levels, we exposed tadpoles of four species of frogs--spring peepers (Pseudacris crucifer), American toads (Bufo americanus, green frogs (Rana clamitans), and wood frogs (Rana sylvatica)--at early and late developmental stages to low concentrations of a commercial preparation of atrazine (3, 30, or 100 ppb; the U.S. Environmental Protection Agency drinking water standard is 3 ppb). We found counterintuitive patterns in rate of survivorship. Survival was significantly lower for all animals exposed to 3 ppb compared with either 30 or 100 ppb, except the late stages of B. americanus and R. sylvatica. These survival patterns highlight the importance of investigating the impacts of contaminants with realistic exposures and at various developmental stages. This may be particularly important for compounds that produce greater mortality at lower doses than higher doses, a pattern characteristic of many endocrine disruptors.

Synergism between trematode infection and pesticide exposure: a link to amphibian limb deformities in nature?

The apparently rapid increase in the prevalence of amphibian limb deformities has led to substantial interest from ecologists and public health professionals. Hypotheses proposed to explain the deformities fall into two broad categories: chemical contaminants and trematode infection. Although there are convincing experimental demonstrations that certain factors can lead to some deformities, the causes for recent increases in amphibian malformation remain controversial. Moreover, no experimental studies on amphibian deformities have been conducted in the field, and no studies have attempted to examine the synergistic effects of trematode infection and exposure to chemical contaminants. Here, I present the results of field and laboratory experiments that link increased trematode infection, and increased limb deformities, to pesticide exposure. Field experiments conclusively demonstrated that exposure to trematode infection was required for the development of limb deformities in wood frogs, Rana sylvatica. However, deformities were more common at sites adjacent to agricultural runoff. Laboratory experiments corroborated the association between pesticide exposure and increased infection with pesticide-mediated immunocompetency as the apparent mechanism. Given the conservative contaminant exposure levels used [Environmental Protection Agency (EPA) drinking water standards] and the widespread use of many pesticides, these negative impacts may help to explain pathogen-mediated amphibian declines in many regions.

Effect of predator diet on life history shifts of red-legged frogs, Rana aurora.

Larval red-legged frogs (Rana aurora) are known to exhibit antipredator behavior in response to both chemical alarm cues released from injured conspecifics and chemical cues of predators. In some cases, the response to predators is dependent on the predator's diet. In this experiment, we tested whether long-term exposure to predator chemical cues and alarm cues resulted in alteration of life history characteristics of red-legged frogs. We raised groups of tadpoles in the presence of chemical cues of predators that were either fed conspecifics or heterospecific caddis-fly larvae, chemical cues of injured conspecifics, or a no-cue control. Tadpoles raised in the presence of either a predator fed conspecifics or cues of injured conspecifics metamorphosed earlier and at a smaller size than those exposed to predators fed heterospecifics or the no-cue control. The result suggests that red-legged frogs exhibit a life history shift in response to predatory cues and that this response is dependent on the diet of predators.

The effects of food level and conspecific density on biting and cannibalism in larval long-toed salamanders, Ambystoma macrodactylum.

Previous studies have examined abiotic and biotic factors that facilitate agonistic behavior. For larval amphibians, food availability and conspecific density have been suggested as important factors influencing intraspecific aggression and cannibalism. In this study, we examined the separate and combined effects of food availability and density on the agonistic behavior and life history of larval long-toed salamanders, Ambystoma macrodactylum. We designed a 2×2 factorial experiment in which larvae were raised with either a high or low density of conspecifics and fed either a high or low level of food. For each treatment, we quantified the amount of group size variation, biting, and cannibalism occurring. Additionally, we examined survival to, time to and size at metamorphosis for all larvae. Results indicated that differences in both density and food level influenced all three life history traits measured. Moreover, differences in food level at which larvae were reared resulted in higher within-group size variation and heightened intraspecific biting while both density and food level contributed to increased cannibalism. We suggest that increased hunger levels and an uneven size structure promoted biting among larvae in the low food treatments. Moreover, these factors combined with a higher encounter rate with conspecifics in the high density treatments may have prompted larger individuals to seek an alternative food source in the form of smaller conspecifics.