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U.S. Geological Survey environmental health science strategy — Providing environmental health science for a changing world

Executive Summary America has an abundance of natural resources. We have bountiful clean water, fertile soil, and unrivaled national parks, wildlife refuges, and public lands. These resources enrich our lives and preserve our health and wellbeing. These resources have been maintained because of our history of respect for their value and an enduring commitment to their vigilant protection. Awareness of the social, economic, and personal value of the health of our environment is increasing. The emergence of environmentally driven diseases caused by exposure to contaminants and pathogens is a growing concern worldwide. New health threats and patterns of established threats are affected by both natural and anthropogenic changes to the environment. Human activities are key drivers of emerging (new and re-emerging) health threats. Societal demands for land and natural resources, quality of life, and economic prosperity lead to environmental change. Natural earth processes, climate trends, and related climatic events will compound the environmental impact of human activities. These environmental drivers will influence exposure to disease agents, including viral, bacterial, prion, and fungal pathogens, parasites, synthetic chemicals and substances, natural earth materials, toxins, and other biogenic compounds. The U.S. Geological Survey (USGS) defines environmental health science broadly as the interdisciplinary study of relations among the quality of the physical environment, the health of the living environment, and human health. The interactions among these three spheres are driven by human activities, ecological processes, and natural earth processes; the interactions affect exposure to contaminants and pathogens and the severity of environmentally driven diseases in animals and people. This definition provides USGS with a framework for synthesizing natural science information from across the Bureau and providing it to environmental, natural resource, agricultural, and public health managers. USGS specializes in science at the environment-health interface, by characterizing the processes that affect the interaction among the physical environment, the living environment, and people, and the resulting factors that affect ecological and human exposure to disease agents. The USGS is a Federal science agency with a broad range of natural science expertise relevant to environmental health. USGS provides scientific information and tools as a scientific basis for management and policy decisionmaking. This report describes a 10-year strategy that encompasses the portfolio of USGS environmental health science. It summarizes national environmental health priorities that USGS is best suited to address, and will serve as a strategic framework for USGS environmental health science goals, actions, and outcomes for the next decade. Implementation of this strategy is intended to aid coordination of USGS environmental health activities and to provide a focal point for disseminating information to stakeholders. The “One Health” paradigm advocated by the World Health Organization (WHO; World Health Organization, 2011), and the American Veterinary Medical Association (AVMA; American Veterinary Medical Association, 2008), among others, is based on a general recognition that the health of humans, animals, and the environment are inextricably linked. Thus, successful efforts to protect that health will require increased interdisciplinary research and increased communication and collaboration among the broader scientific and health community. This strategy is built upon that paradigm.

Circular

Intraspecific and biogeographical variation in foliar fungal communities and pathogen damage of native and invasive Phragmites australis

Aim Recent research has highlighted that the relationship between species interactions and latitude can differ between native and invasive plant taxa, generating biogeographical heterogeneity in community resistance to plant invasions. In the first study with foliar pathogens, we tested whether co‐occurring native and invasive lineages of common reed ( Phragmites australis ) exhibit non‐parallel latitudinal gradients in foliar fungal communities, pathogen susceptibility and damage, and whether these biogeographical patterns can influence the success of invasion. Location North America. Time period 2015–2017. Major taxa studied Perennial grass P. australis . Methods We surveyed 35 P. australis field populations, spanning 17° latitude and comprising four phylogeographical lineages, including one endemic to North America and one invasive from Europe. For each population, we quantified the percentage of leaf pathogen damage and cultured fungi from diseased leaves, which we identified using molecular tools. To assess whether latitudinal gradients in pathogen damage had a genetic basis, we inoculated plants from 73 populations with four putative pathogens in a complementary common garden experiment and measured P. australis susceptibility (i.e., diseased leaf area). Results We isolated 84 foliar fungal taxa. Phragmites australis lineage influenced fungal community composition but not diversity. Despite the invasive European P. australis lineage being the least susceptible to three of the four pathogens tested in the common garden experiment, pathogen damage in the field was similar between native and invasive lineages, providing no evidence that release from foliar pathogens contributes to the success of invasion. Genetically based latitudinal gradients in pathogen susceptibility observed in the common garden were isolate specific and obscured by local environmental conditions in the field, where pathogen damage was threefold higher for northern compared with southern populations, regardless of lineage. Main conclusions Our results highlight that host plant lineage and genetically based biogeographical gradients strongly influence foliar fungal communities and pathogen susceptibility, but do not translate to patterns of pathogen damage observed in the field.

Global Ecology and Biogeography

USGS Environmental health science strategy: providing environmental health science for a changing world: Public review release

America has an abundance of natural resources. We have bountiful clean water, fertile soil, and unrivaled national parks, wildlife refuges, and public lands. These resources enrich our lives and preserve our health and wellbeing. These resources have been maintained because of our history of respect for their value and an enduring commitment to their vigilant protection. Awareness of the social, economic, and personal value of the health of our environment is increasing. The emergence of environmentally driven diseases caused by environmental exposure to contaminants and pathogens is a growing concern worldwide. New health threats and patterns of established threats are affected by both natural and anthropogenic changes to the environment. Human activities are key drivers of emerging (new and re-emerging) health threats. Societal demands for land and natural resources, a better quality of life, improved economic prosperity, and the environmental impacts associated with these demands will continue to increase. Natural earth processes, climate trends, and related climatic events will add to the environmental impact of human activities. These environmental drivers will influence exposure to disease agents, including viral, bacterial, prion, and fungal pathogens, parasites, natural earth materials, toxins and other biogenic compounds, and synthetic chemicals and substances. The U.S. Geological Survey (USGS) defines environmental health science broadly as the interdisciplinary study of relations among the quality of the physical environment, the health of the living environment, and human health. The interactions among these three spheres are driven by human activities, ecological processes, and natural earth processes; the interactions affect exposure to contaminants and pathogens and the severity of environmentally driven diseases in animals and people. This definition provides USGS with a framework for synthesizing natural science information from across the Bureau and providing it to environmental, natural resource, agricultural, and public-health managers. The USGS is a Federal science agency with a broad range of natural science expertise relevant to environmental health. USGS provides scientific information and tools as a scientific basis for management and policy decision making. USGS specializes in science at the environment-health interface, by characterizing the processes that affect the interaction among the physical environment, the living environment, and people, and the resulting factors that affect ecological and human exposure to disease agents. This report describes a 10-year strategy that encompasses the portfolio of USGS environmental health science. It summarizes national environmental health priorities that USGS is best suited to address, and will serve as a strategic framework for USGS environmental health science goals, actions, and outcomes for the next decade. Implementation of this strategy is intended to aid coordination of USGS environmental health activities and to provide a focal point for disseminating information to stakeholders. The "One Health" paradigm advocated by the World Health Organization (WHO, 2011), and the American Veterinary Medicine Association (AVMA, 2008), among others, is based on a general recognition that the health of humans, animals, and the environment are inextricably linked. Thus, successful efforts to protect that health will require increased interdisciplinary research and increased communication and collaboration among the broader scientific and health community. This strategy is built upon that paradigm. The vision, mission, and five cornerstone goals of the USGS Environmental Health Science Strategy were developed with significant input from a wide range of stakeholders. Vision - The USGS is a premier source of the environmental health science needed to safeguard the health of the environment, fish, wildlife, and people. Mission - The mission of USGS in environmental health science is to contribute scientific information to environmental, natural resource, agricultural, and public-health managers, who use that science to support sound decision making. USGS provides the science to: - Goal 1: Identify, prioritize, and detect contaminants and pathogens of emerging environmental concern. - Goal 2: Reduce the impact of contaminants on the environment, fish, wildlife, and people. - Goal 3: Reduce the impact of pathogens on the environment, fish, wildlife, and people. - Goal 4: Discover the complex interactions and combined effects of exposure to contaminants and pathogens. - Goal 5: Prepare for and respond to environmental impacts and related health threats of natural and anthropogenic disasters. Goals 1 through 4 are intended to provide science to address environmental health threats in a logical order, from informing prevention and preparedness, to supporting systematic management response to environmental health issues. Goal 4 addresses the interaction among contaminants and pathogens, an issue of emerging concern in environmental health science. Goal 5 acknowledges the fact that natural and anthropogenic disasters can cause immediate and prolonged adverse environmental health threats. This strategy proposes that USGS take the following strategic science actions to achieve each of the five goals of this strategy: Goal 1: Identify, prioritize, and detect contaminants and pathogens of emerging environmental concern. - Strategic Science Action 1. - Prioritize contaminants and pathogens of emerging concern to guide research, detection, and management activities. - Strategic Science Action 2. - Conduct surveillance and monitoring to provide early warning of emerging health threats. - Strategic Science Action 3. - Develop approaches and tools that identify vulnerable environmental settings, ecosystems, and species. Goal 2: Reduce the impact of contaminants on the environment, fish, wildlife, and people. - Strategic Science Action 1. - Systematically characterize the sources, occurrence, transport and fate of environmental contaminants to guide efforts to manage and mitigate contamination. - Strategic Science Action 2. - Evaluate the threats of contamination on the health of the environment, fish, wildlife, and people, and inform the associated management and protection efforts. - Strategic Science Action 3. - Characterize potential human exposure to support establishment of health-based standards or guidelines and contamination-reduction efforts. Goal 3: Reduce the impact of pathogens on the environment, fish, wildlife, and people. - Strategic Science Action 1. - Determine the biotic and abiotic factors that control the ecology of infectious diseases affecting natural populations of aquatic and terrestrial species and potential transmission to other animals and humans. - Strategic Science Action 2. - Establish how natural and anthropogenic environmental changes affect the distribution and severity of infectious diseases in natural populations of aquatic and terrestrial species and potential transmission to other animals and humans. - Strategic Science Action 3. - Develop surveillance systems to identify changing patterns of disease activity in priority geographic areas. Goal 4: Discover the complex interactions and combined effects of exposure to contaminants and pathogens. - Strategic Science Action 1. - Identify how exposure to one class of disease agents (contaminants or pathogens) can make an organism more susceptible to effects from exposure to the other class of disease agents. - Strategic Science Action 2. - Implement interdisciplinary studies that characterize the effects of combined exposure to pathogens and contaminants. Goal 5: Prepare for and respond to the environmental impacts and related health threats of natural and anthropogenic disasters. - Strategic Science Action 1. - Establish a formal interdisciplinary science capability to rapidly assess the environmental health risks associated with disasters. - Strategic Science Action 2. - Enhance methods to anticipate, prepare for, and identify environmental, ecological, and related health impacts of future disasters. This strategy is one of seven USGS science strategies developed concurrently: - Climate and Land Use Change - Core Science Systems - Ecosystems - Energy and Mineral Resources - Environmental Health - Natural Hazards - Water. This strategy describes how USGS will address the highest priority environmental health issues facing the Nation. The ultimate intended outcome of this science strategy is prevention and reduction of adverse impacts to the quality of the environment, the health of our living resources, and human health. Communication with, and receiving input from, partners and stakeholders regarding their science needs is essential for successful implementation of this strategy. It is incumbent on USGS to reach out to all stakeholders to ensure that USGS efforts are focused on the highest priority environmental health issues and that products are provided in the most timely and usable form to all those who can use them. USGS must reach out to the scientific community, internally and externally, to ensure that our efforts are integrated with and take full advantage of the activities of others.

Open-File Report

Experimental drought suppresses amphibian pathogen yet intensifies transmission and disrupts protective skin microbiome

Shifting precipitation regimes driven by global climate change can alter vertebrate behavior and host-symbiont relationships, potentially compromising host resistance to pathogen invasion. In Brazil's Atlantic Forest, a biodiversity hotspot, prior research identified drought as a key factor disrupting the skin microbiome, contributing to a die-off of pumpkin toadlets due to the invasive waterborne fungal pathogen Batrachochytrium dendrobatidis (Bd). However, observational studies cannot disentangle the direct effect of moisture on Bd growth from increased amphibian activity during wet breeding seasons. Using field enclosures, we experimentally tested the influence of drought conditions on host microhabitat use, Bd disease dynamics, and the composition and predicted Bd-inhibitory function of cutaneous bacterial communities. Each enclosure housed ecologically realistic densities of Brachycephalus pitanga , a micro-endemic pumpkin toadlet. We simulated a short-term drought in half of the enclosures using translucent tarp coverings. To track individual toadlets, we identified their unique markings and collected skin swabs biweekly over 3 months. We then implemented molecular techniques to quantify Bd loads and characterize skin bacterial diversity and composition over time. Our findings indicate that while drought may reduce overall Bd loads on hosts, this effect is partially offset by an increase in the use of water-filled areas of the enclosures and by a disruption of the protective host skin microbiome. This study provides valuable insights into the cascading impacts of climate change on animal behavior, host-symbiont interactions, and disease dynamics.

Atlantic Forest

Effect of permafrost thaw on plant and soil fungal community in the boreal forest: Does fungal community change mediate plant productivity response?

Permafrost thaw is leading to rapid shifts in boreal ecosystem function. Permafrost thaw affects soil carbon turnover through changes in soil hydrology, however, the biotic mechanisms regulating plant community response remain elusive. Here, we measured the response of fungal community composition and soil nutrient content in an intact permafrost plateau forest soil and an adjacent thermokarst bog using barcoded amplicon targeting ITS2 and 28S rRNA genes. Next, we used the soils from the permafrost plateau and the thermokarst bog as soil inoculum in a greenhouse experiment to measure whether shifts in fungal community and soil water level regulate plant productivity. Overall, we found that fungal community composition differed significantly between the thawed and intact permafrost sites, but soil nutrient content did not. Relative abundance of mycorrhizal fungal taxa decreased while relative abundance of putative fungal pathogens increased with permafrost thaw. In the greenhouse, we found that ecto- and arbuscular associated host plants had higher productivity in permafrost-intact soils relative to thawed soils. However, productivity of non-mycorrhizal tussock grass was more affected by soil water levels than soil communities. Our results suggest that fungal communities are crucial in mediating plant response to permafrost thaws inducing hydrology changes.

Alaska

Low-level detection of SFD-causing Ophidiomyces on Burmese Pythons in southwest Florida, with confirmation of the pathogen on co-occurring native snakes

Snake fungal disease (SFD), or ophidiomycosis, is caused by the fungus Ophidiomyces ophiodiicola (Allender et al. 2015; Lorch et al. 2015). SFD is widespread across wild populations in the eastern United States (Lorch et al. 2016) and is known to infect more than 30 species of snake in North America and Europe (Lorch et al. 2016; Franklinos et al. 2017). No known phylogenetic or ecological patterns have been observed in susceptibility among snake taxa, and it is presumed that all species are likely susceptible (Burbrink et al. 2017).

Florida

Pan-amphibia distribution of the fungal parasite Batrachochytrium dendrobatidis varies with species and temperature

Batrachochytrium dendrobatidis (Bd) is a globally distributed fungal pathogen of amphibians that has contributed to one of the largest disease-related biodiversity losses in wildlife. Bd is regularly viewed through the lens of a global wildlife epizootic because the spread of highly virulent genetic lineages has resulted in well-documented declines and extinctions of multiple amphibian species. However, the current state of Bd occurrence, host range, host impacts, and ecological drivers remains poorly understood outside of the most negatively affected amphibian species and regions. Our objective was to describe the macroecology of Bd occurrence and infection intensity on caudates (salamanders) across the United States and to compare these patterns with better-studied anurans (frogs and toads). We collected swabs from 11,183 amphibians at 609 sites from 54 species across the United States from 2015 to 2017. We analyzed the prevalence and intensity of Bd infection jointly using a Bayesian hurdle model with covariates of site-level temperature and precipitation, as well as individual characteristics and species identification. Bd was distributed widely across sites and species sampled across the spatial extent of the conterminous United States. We found that Bd prevalence and intensity were most strongly influenced by temperature in the month preceding sampling and by differences among taxon groups. We estimated that temperature had a strong and nonlinear influence on both Bd prevalence and intensity with peak infection at intermediate temperatures and lower infection at low and high temperatures. We found Caudate hosts tended to have higher prevalence than Anuran hosts and Anuran hosts tended to have higher intensity at optimal temperatures for Bd infection. Our findings suggest that Bd has an amphibian-wide host range, temperature gradients exert a strong influence on Bd, and enzootic transmission likely encompasses a much larger spatial and species distribution than previously recognized across North America.

conterminous United States

Spatial variation in risk and consequence of Batrachochytrium salamandrivorans introduction in the USA

A newly identified fungal pathogen, Batrachochytrium salamandrivorans ( Bsal ), is responsible for mass mortality events and severe population declines in European salamanders. The eastern USA has the highest diversity of salamanders in the world and the introduction of this pathogen is likely to be devastating. Although data are inevitably limited for new pathogens, disease-risk assessments use best available data to inform management decisions. Using characteristics of Bsal ecology, spatial data on imports and pet trade establishments, and salamander species diversity, we identify high-risk areas with both a high likelihood of introduction and severe consequences for local salamanders. We predict that the Pacific coast, southern Appalachian Mountains and mid-Atlantic regions will have the highest relative risk from Bsal . Management of invasive pathogens becomes difficult once they are established in wildlife populations; therefore, import restrictions to limit pathogen introduction and early detection through surveillance of high-risk areas are priorities for preventing the next crisis for North American salamanders.

Royal Society Open Science

Global trends in emerging viral diseases of wildlife origin

Fifty years ago, infectious diseases were rarely considered threats to wildlife populations, and the study of wildlife diseases was largely a neglected endeavor. Furthermore, public health leaders at that time had declared that “it is time to close the book on infectious diseases and the war against pestilence won,” a quote attributed to Dr. William H. Stewart in 1967. There is some debate whether he actually said these words; however, they reflect the widespread belief at that time (Spellberg, 2008). Leap forward to today, and the book on infectious diseases has been dusted off. There is general consensus that the global environment favors the emergence of infectious diseases, and in particular, diseases of wildlife origin (Taylor et al., 2001). Examples of drivers of these infectious diseases include climate and landscape changes, human demographic and behavior changes, global travel and trade, microbial adaptation, and lack of appropriate infrastructure for wildlife disease control and prevention (Daszak et al., 2001). The consequences of these emerging diseases are global and profound with increased burden on the public health system, negative impacts on the global economy and food security, declines and extinctions of wildlife species, and subsequent loss of ecosystem integrity. For example, 35 million people are currently living with HIV infection globally (http://www.who.int/gho/hiv/en); 400 million poultry have been culled since 2003 as a result of efforts to control highly pathogenic H5N1 avian influenza (http://www.fao.org/avianflu/en/index.html), and there are increasing biological and ecological consequences. Examples of health threats to biodiversity include the “spillover” of human diseases to great ape populations (Köndgen et al., 2008), the near-extirpation of the black-footed ferret from canine distemper and sylvatic plague (for a review see Abbott et al., 2012), and threats to Hawaiian forest birds from introduced pathogens such as avian malaria and avian pox (van Riper et al., 1986, 2002). There are also newly discovered pathogens or diseases that have resulted in population declines, and global extinctions of several species. Examples include Batrachochytrium dendrobatidis, which causes a cutaneous fungal infection of amphibians and is linked to declines of amphibians globally (Kriger and Hero, 2009); and recently discovered Pseudogymnoascus (Geomyces) destructans, the etiologic agent of white-nose syndrome (WNS), which has caused precipitous declines of North American bat species (Blehert et al., 2009). Furthermore, there is increasing evidence of the subsequent impacts on human and ecosystem health; for example, increasing risk of exposure to Lyme disease as a consequence of decreased biodiversity (LoGiudice et al., 2003) as well as the economic cost of the loss of bats due to decreased insect control services (Boyles et al., 2011). Figure A12-1 is a timeline of important diseases investigated by the U.S. Geological Survey since the 1970s, which illustrates three factors: 1. The unprecedented emergence of new pathogens and geographic spread of known pathogens since the 1990s; 2. Diseases are increasingly causing large-scale, negative impacts on wildlife populations and spreading over larger geographic areas rather than remaining localized; and 3. Diseases are increasingly of concern for multiple sectors, including public health, agriculture and wildlife management agencies. Of increasing concern are these novel diseases such as WNS as they are hard to anticipate, particularly devastating to human health or wildlife populations, challenging to manage, spread over large geographic areas in short time periods, and may result in ecological ripple effects that are difficult to predict. The following article provides examples of recently emerged viral diseases of wildlife origin. The examples have been selected to illustrate the drivers of emerging viral diseases, both novel pathogens and previously known diseases, the impacts of these diseases, as well as the role of wildlife both as “villains” or reservoirs as well as “victims” of these viral diseases. The article also discusses potential management strategies for emerging viral diseases in wildlife populations and future science directions in wildlife health to prevent, prepare, respond to, and recover from these disease events. Finally, the concept of One Health and its potential role in developing solutions to these issues of mutual concern is discussed.

Conference Paper

Weather and distance to fire refugia limit landscape‐level occurrence of fungal disease in an exotic annual grass

The enemy release hypothesis proposes that invasion by exotic plant species is driven by their release from natural enemies (i.e. herbivores and pathogens) in their introduced ranges. However, in many cases, natural enemies, which may be introduced or managed to regulate invasive species, may fail to impact target host populations. Landscape heterogeneity, which can affect both the population dynamics of the pathogen and the susceptibility and the density of hosts, may contribute to why pathogens fail to control hosts despite established negative disease impacts. We explored patterns of post‐fire infection of the fungal head‐smut pathogen Ustilago bullata on the invasive annual cheatgrass Bromus tectorum , which has caused the notorious grass‐fire cycle and ecosystem degradation across Western North America. We asked whether infection level was a driver of host density or vice‐versa, and how weather affected infection and how spatial patterns of infection varied with time since fire, using a combination of structural equation modelling (SEM), proportional odds modelling and entropy‐based local indicator of spatial association (ELSA) on data from >700 plots spanning >100,000 ha remeasured annually for 4 years. Observed infection levels increased with greater prior‐year cheatgrass cover, and disease severity did not suppress cheatgrass populations. Warm, humid fall/winters and proximity to fire refugia (unburned patches) were associated with more infections. Infection clustering was most evident 2–3 years following fire with warm‐wet fall–winter conditions and decreased after two drier, colder winters. Synthesis . Severity of fungal disease did not result in measurable reductions of populations of a non‐native, invasive host species, cheatgrass, which suggests that natural enemies may not strongly regulate cheatgrass in its introduced range. Landscape heterogeneity associated with disturbance and weather limited population‐level infection of hosts by the fungal pathogen. Disturbance (specifically wildfire) and variable weather are key components of this and similar invasion systems, and likely need to be considered when evaluating disease dynamics and potential for natural enemies to influence invasion potential.

Journal of Ecology

Chiroptera

With over 1200 species identified, bats represent almost one quarter of the world’s mammals. Bats provide crucial environmental services, such as insect control and pollination, and inhabit a wide variety of ecological niches on all continents except Antarctica. Despite their ubiquity and ecological importance, relatively little has been published on diseases of bats, while much has been written on bats’ role as reservoirs in disease transmission. This chapter will focus on diseases and pathologic processes most commonly reported in captive and free-ranging bats. Unique anatomical and histological features and common infectious and non-infectious diseases will be discussed. As recognition of both the importance and vulnerability of bats grows, particularly following population declines in North America due to the introduction of the fungal disease white-nose syndrome, efforts should be made to better understand threats to the health of this unique group of mammals.

Book chapter

Ecological implications of Laurel Wilt infestation on Everglades Tree Islands, southern Florida

There is a long history of introduced pests attacking native forest trees in the United States (Liebhold and others, 1995; Aukema and others, 2010). Well-known examples include chestnut blight that decimated the American chestnut ( Castanea dentata ), an extremely important tree in the eastern United States, both as a food source for wildlife and humans and for the wood; Dutch elm disease that attacks native elms ( Ulmus spp.), including those commonly planted as shade trees along city streets; and the balsam wooly adelgid (Adelges piceae), an insect that is destroying Fraser firs ( Abies fraseri ) in higher elevations of Great Smoky Mountains National Park. Laurel wilt, a fungal disease transmitted by the redbay ambrosia beetle (Xyleborus glabratus), is a 21st-century example of an introduced forest pest that attacks native tree species in the laurel family (Lauraceae) (Mayfield, 2007; Hulcr and Dunn, 2011). The introduction of laurel wilt disease has been traced to the arrival of an Asian ambrosia beetle ( Xyleborus glabratus ) at Port Wentworth, Georgia, near Savannah, in 2002, apparently accidently introduced in wooden shipping material (Mayfield, 2007). Within the next 2 years, it was determined that the non-native wood-boring insect was the vector of an undescribed species of fungus, responsible for killing large numbers of red bay ( Persea borbonia ) trees in the surrounding area. Dispersing female redbay ambrosia beetles drill into live trees and create tunnels in the wood. They carry with them fungal spores in specialized organs called mycangia at the base of each mandible and sow the spores in the tunnels they excavate. The fungus, since named Raffaelea lauricola (Harrington and others, 2008), is the food source for adults and larvae. The introduction of Raffaelea lauricola causes the host plant to react in such a way as to block the vascular tissue, resulting in loss of water conduction, wilt, and death (Kendra and others, 2013). Although first seen in red bay, laurel wilt disease also kills other native trees that are members of the laurel family, including swamp bay ( Persea palustris ), silk bay ( Persea borbonia var. humilis ), and sassafras ( Sassafras albidum ), as well as the economically important cultivated avocado ( Persea americana ) (Fraedrich and others, 2008). This paper is concerned primarily with swamp bay, an important component of Everglades tree islands. The spread of the redbay ambrosia beetle and its fungal symbiont has been very rapid, exceeding model predictions (Koch and Smith, 2008); by 2011, laurel wilt disease was found from the southern coastal plain of North Carolina to southern peninsular Florida. The first redbay ambrosia beetle was trapped in Miami-Dade County in March 2010, and laurel wilt disease was discovered in swamp bays in February 2011 and in commercial avocado groves about a year later (Kendra and others, 2013). By 2013, laurel wilt disease was seen in swamp bays throughout the southern Everglades in Everglades National Park, Big Cypress National Preserve, and Water Conservation Areas (WCAs) 3A and 3B (Rodgers and others, 2014).

Florida

Leaf litter decomposition and detrital communities following the removal of two large dams on the Elwha River (Washington, USA)

Large-scale dam removals provide opportunities to restore river function in the long-term and are massive disturbances to riverine ecosystems in the short-term. The removal of two dams on the Elwha River (WA, USA) between 2011 and 2014 was the largest dam removal project to be completed by that time and has since resulted in major changes to channel dynamics, river substrates, in-stream communities, and the size and shape of the river delta. To assess ecosystem function across the restored Elwha watershed, we compared leaf litter decomposition at twenty sites: 1) four tributary sites not influenced by restoration activities; 2) four river sites downstream of the upper dam (Glines Canyon Dam); 3) four river sites within the footprint of the former Aldwell Reservoir upstream of the lower dam (Elwha Dam); 4) four river sites downstream of the lower dam; and 5) four lentic sites in the newly developing Elwha delta. Three major findings emerged: 1) decomposition rates differed among sections of the Elwha watershed, with slowest decomposition rates at the delta sites and fastest decomposition rates just downstream of the upper dam; 2) aquatic macroinvertebrate communities establishing in leaf litterbags differed significantly among sections of the Elwha watershed; and 3) aquatic fungal communities growing on leaf litter differed significantly among sections. Aquatic macroinvertebrate and fungal diversity were sensitive to differences in canopy cover, water chemistry, and river bottom sediments across sites, with a stronger relationship to elevation for aquatic macroinvertebrates. As the Elwha River undergoes recovery following the massive sediment flows associated with dam removal, we expect to see changes in leaf litter processing dynamics and shifts in litter-dependent decomposer communities (both fungal and invertebrate) involved in this key ecosystem process.

Washington

Influence of soil microbiota on Taxodium distichum seedling performance during extreme flooding events

Plant associations with soil microbiota can modulate tree seedling growth and survival via mutualistic or antagonistic interactions. It is uncertain, however, whether soil microbiota influence seedling growth of coastal trees when exposed to extreme flooding regimes. We evaluated the role of soil microbes in promoting baldcypress ( Taxodium distichum ) seedling performance under different inundation scenarios and determined the influence of flooding on the colonization of in planta beneficial microbes. Seedlings reared in sterile and non-sterile soil were exposed to three different flooding regimes historically experienced in Louisiana swamps. Seedling growth was assessed, and the colonization by beneficial symbionts such as arbuscular mycorrizhal fungi (AMF), and dark septate endophytes (DSE) was evaluated in harvested roots. Seedlings grown in sterile soil had six times higher growth than seedlings reared in non-sterile soil. As a result, we evaluated pathogen load in the roots by assessing oomycete colonization. Flooding influenced the in planta colonization of DSE and oomycetes, but did not affect the colonization of mutualist AMF fungi. DSE and oomycetes were rarer in flooded conditions, while AMF remained abundant. Seedling biomass production was not correlated with in planta fungal colonization or pathogen load. Soil microbiota can negatively influence baldcypress seedling growth, and no growth benefit was evidenced from the root colonization of mutualist fungi. Flooding can modify baldcypress-fungal interactions by diminishing colonization of DSE. Overall, baldycpress seedlings were more sensitive to the presence of microbiota than flooding, and thus restoration efforts should focus on having a better understanding of plant–microbe interactions in swamps.

Louisiana

A meta-analysis highlights the idiosyncratic nature of tradeoffs in laboratory models of virus evolution

Different theoretical frameworks have been invoked to guide the study of virus evolution. Three of the more prominent ones are (i) the evolution of virulence, (ii) life history theory, and (iii) the generalism–specialism dichotomy. All involve purported tradeoffs between traits that define the evolvability and constraint of virus-associated phenotypes. However, as popular as these frameworks are, there is a surprising paucity of direct laboratory tests of the frameworks that support their utility as broadly applicable theoretical pillars that can guide our understanding of disease evolution. In this study, we conduct a meta-analysis of direct experimental evidence for these three frameworks across several widely studied virus–host systems: plant viruses, fungal viruses, animal viruses, and bacteriophages. We extracted 60 datasets from 28 studies and found a range of relationships between traits in different analysis categories (e.g., frameworks, virus–host systems). Our work demonstrates that direct evidence for relationships between traits is highly idiosyncratic and specific to the host–virus system and theoretical framework. Consequently, scientists researching viral pathogens from different taxonomic groups might reconsider their allegiance to these canons as the basis for expectation, explanation, or prediction. Future efforts could benefit from consistent definitions, and from developing frameworks that are compatible with the evidence and apply to particular biological and ecological contexts.

Virus Evolution

Learning complex spatial dynamics of wildlife diseases with machine learning-guided partial differential equations

Emerging wildlife pathogens often display geographic variability due to landscape heterogeneity. Modeling approaches capable of learning complex, non-linear spatial dynamics of diseases are needed to rigorously assess and mitigate the effects of pathogens on wildlife health and biodiversity. We propose a novel machine learning (ML)-guided approach that leverages prior physical knowledge of ecological systems, using partial differential equations. We present our approach, taking advantage of the universal function approximation property of neural networks for flexible representation of the underlying dynamics of the geographic spread and growth of wildlife diseases. We demonstrate the benefits of our approach by comparing its forecasting power with commonly used methods and highlighting the obtained insights on disease dynamics. Additionally, we show the theoretical guarantees for the approximation error of our model. We illustrate the implementation of our ML-guided approach using data from white-nose syndrome (WNS) outbreaks in bat populations across the US. WNS is an infectious fungal disease responsible for significant declines in bat populations. Our results on WNS are useful for disease surveillance and bat conservation efforts. Our methods can be broadly used to assess the effects of environmental and anthropogenic drivers impacting wildlife health and biodiversity.

Environmental Data Science

Nonstationary demographic state-space models using unreplicated counts for species undergoing environmental stressors

A fundamental task in ecological statistics is to estimate abundance and growth rate distributions from wildlife monitoring data to inform conservation management. Modeling time series of wildlife populations presents a number of challenges from both statistical and ecological perspectives, including discreteness; lack of replication; nonstationarity; and observation, demographic, and other phenomenological processes. Nonstationary dynamics are often exhibited by populations undergoing environmental stressors. Models must account for these characteristics to produce reliable estimates of abundance and trends, yet estimation can be challenging with unreplicated data. We propose nonstationary demographic state-space models using unreplicated counts for populations undergoing environmental stressors. A reduced growth rate model matches the complexity of the unreplicated count data, and a fecundity bound on growth rate distributions allows the separation of processes affecting growth rates like environmental stressors from those affecting abundance external to growth rates like migration. NDSSMs allow for the embedding of nonstationary model components, and we explore the use of changepoints, volatility clustering, and migration processes. We apply the proposed nonstationary models in case studies of herons affected by predator/competitor reestablishment and three bat species affected by a fungal pathogen causing white-nose syndrome. Nonstationary models outperform stationary models and generalized linear mixed effects models according to model scoring and visual inspection of predictions, and provide estimates more consistent with published values. Incorporating migration improves model fit universally, even with approximate one-way immigration, most likely because populations are extirpated, recolonized, and increase multiple-fold over the upper bound set by species fecundity. In addition, estimates of the timing and severity of the environmental stressor differed for models with migration. Including nonstationary and demographic components in a fecundity-bounded growth rate model improves inference and benefits interpretability of hyperparameters. In turn, this adjusts uncertainties in predictions of abundance and growth rates over time, providing the ingredients needed for informed conservation analysis and for directing future monitoring of at-risk species.

Journal of Agricultural, Biological and Environmen

Mast seeding in European beech (Fagus sylvatica L.) is associated with reduced fungal sporocarp production and community diversity

Mast seeding is a well-documented phenomenon across diverse forest ecosystems. While its effect on aboveground food webs has been thoroughly studied, how it impacts the soil fungi that drive soil carbon and nutrient cycling has not yet been explored. To evaluate the relationship between mast seeding and fungal resource availability, we paired a Swiss 29-year fungal sporocarp census with contemporaneous seed production for European beech ( Fagus sylvatica L.). On average, mast seeding was associated with a 55% reduction in sporocarp production and a compositional community shift towards drought-tolerant taxa across both ectomycorrhizal and saprotrophic guilds. Among ectomycorrhizal fungi, traits associated with carbon cost did not explain species' sensitivity to seed production. Together, our results support a novel hypothesis that mast seeding limits annual resource availability and reproductive investment in soil fungi, creating an ecosystem ‘rhythm’ to forest processes that is synchronized above- and belowground.

Ecology Letters