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USGS2011

Mitigating amphibian disease: strategies to maintain wild populations and control chytridiomycosis

Background Rescuing amphibian diversity is an achievable conservation challenge. Disease mitigation is one essential component of population management. Here we assess existing disease mitigation strategies, some in early experimental stages, which focus on the globally emerging chytrid fungus Batrachochytrium dendrobatidis . We discuss the precedent for each strategy in systems ranging from agriculture to human medicine, and the outlook for each strategy in terms of research needs and long-term potential. Results We find that the effects of exposure to Batrachochytrium dendrobatidis occur on a spectrum from transient commensal to lethal pathogen. Management priorities are divided between (1) halting pathogen spread and developing survival assurance colonies, and (2) prophylactic or remedial disease treatment. Epidemiological models of chytridiomycosis suggest that mitigation strategies can control disease without eliminating the pathogen. Ecological ethics guide wildlife disease research, but several ethical questions remain for managing disease in the field. Conclusions Because sustainable conservation of amphibians in nature is dependent on long-term population persistence and co-evolution with potentially lethal pathogens, we suggest that disease mitigation not focus exclusively on the elimination or containment of the pathogen, or on the captive breeding of amphibian hosts. Rather, successful disease mitigation must be context specific with epidemiologically informed strategies to manage already infected populations by decreasing pathogenicity and host susceptibility. We propose population level treatments based on three steps: first, identify mechanisms of disease suppression; second, parameterize epizootiological models of disease and population dynamics for testing under semi-natural conditions; and third, begin a process of adaptive management in field trials with natural populations.

Frontiers in Zoology↗

USGS2010

Meeting report: knowledge and gaps in developing microbial criteria for inland recreational waters

The U.S. Environmental Protection Agency (EPA) has committed to issuing in 2012 new or revised criteria designed to protect the health of those who use surface waters for recreation. For this purpose, the U.S. EPA has been conducting epidemiologic studies to establish relationships between microbial measures of water quality and adverse health outcomes among swimmers. New methods for testing water quality that would provide same-day results will likely be elements of the new criteria. Although the epidemiologic studies upon which the criteria will be based were conducted at Great Lakes and marine beaches, the new water quality criteria may be extended to inland waters (IWs). Similarities and important differences between coastal waters (CWs) and IWs that should be considered when developing criteria for IWs were the focus of an expert workshop. Here, we summarize the state of knowledge and research needed to base IWs microbial criteria on sound science. Two key differences between CWs and IWs are the sources of indicator bacteria, which may modify the relationship between indicator microbes and health risk, and the relationship between indicators and pathogens, which also may vary within IWs. Monitoring using rapid molecular methods will require the standardization and simplification of analytical methods, as well as greater clarity about their interpretation. Research needs for the short term and longer term are described.

Environmental Health Perspectives↗

USGS2011

Simulating sterilization, vaccination, and test-and-remove as brucellosis control measures in bison

Brucella abortus, the causative agent of bovine brucellosis, infects wildlife, cattle, and humans worldwide, but management of the disease is often hindered by the logistics of controlling its prevalence in wildlife reservoirs. We used an individually based epidemiological model to assess the relative efficacies of three management interventions (sterilization, vaccination, and test-and-remove). The model was parameterized with demographic and epidemiological data from bison in Yellowstone National Park, USA. Sterilization and test-and-remove were most successful at reducing seroprevalence when they were targeted at young seropositive animals, which are the most likely age and sex category to be infectious. However, these approaches also required the most effort to implement. Vaccination was less effective (even with a perfect vaccine) but also required less effort to implement. For the treatment efforts we explored (50–100 individuals per year or 2.5–5% of the female population), sterilization had little impact upon the bison population growth rate when selectively applied. The population growth rate usually increased by year 25 due to the reduced number of Brucella-induced abortions. Initial declines in seroprevalence followed by rapid increases (>15% increase in 5 years) occurred in 3–13% of simulations with sterilization and test-and-remove, but not vaccination. We believe this is due to the interaction of superspreading events and the loss of herd immunity in the later stages of control efforts as disease prevalence declines. Sterilization provided a mechanism for achieving large disease reductions while simultaneously limiting population growth, which may be advantageous in some management scenarios. However, the field effort required to find the small segment of the population that is infectious rather than susceptible or recovered will likely limit the utility of this approach in many free-ranging wildlife populations. Nevertheless, we encourage scientists and policy makers to consider sterilization as part of a suite of available brucellosis management tools.

Ecological Applications↗

USGS2013

Is exposure to cyanobacteria an environmental risk factor for amyotrophic lateral sclerosis and other neurodegenerative diseases?

There is a broad scientific consensus that amyotrophic lateral sclerosis (ALS) is caused by gene-environment interactions. Mutations in genes underlying familial ALS (fALS) have been discovered in only 5–10% of the total population of ALS patients. Relatively little attention has been paid to environmental and lifestyle factors that may trigger the cascade of motor neuron death leading to the syndrome of ALS, although exposure to chemicals including lead and pesticides, and to agricultural environments, smoking, certain sports, and trauma have all been identified with an increased risk of ALS. There is a need for research to quantify the relative roles of each of the identified risk factors for ALS. Recent evidence has strengthened the theory that chronic environmental exposure to the neurotoxic amino acid β-N-methylamino-L-alanine (BMAA) produced by cyanobacteria may be an environmental risk factor for ALS. Here we describe methods that may be used to assess exposure to cyanobacteria, and hence potentially to BMAA, namely an epidemiologic questionnaire and direct and indirect methods for estimating the cyanobacterial load in ecosystems. Rigorous epidemiologic studies could determine the risks associated with exposure to cyanobacteria, and if combined with genetic analysis of ALS cases and controls could reveal etiologically important gene-environment interactions in genetically vulnerable individuals.

Amyotrophic Lateral Sclerosis and Frontotemporal D↗

USGS2012

AquaPathogen X--A template database for tracking field isolates of aquatic pathogens

AquaPathogen X is a template database for recording information on individual isolates of aquatic pathogens and is available for download from the U.S. Geological Survey (USGS) Western Fisheries Research Center (WFRC) website (http://wfrc.usgs.gov). This template database can accommodate the nucleotide sequence data generated in molecular epidemiological studies along with the myriad of abiotic and biotic traits associated with isolates of various pathogens (for example, viruses, parasites, or bacteria) from multiple aquatic animal host species (for example, fish, shellfish, or shrimp). The simultaneous cataloging of isolates from different aquatic pathogens is a unique feature to the AquaPathogen X database, which can be used in surveillance of emerging aquatic animal diseases and clarification of main risk factors associated with pathogen incursions into new water systems. As a template database, the data fields are empty upon download and can be modified to user specifications. For example, an application of the template database that stores the epidemiological profiles of fish virus isolates, called Fish ViroTrak (fig. 1), was also developed (Emmenegger and others, 2011).

Fact Sheet↗

USGS2012

An online database for IHN virus in Pacific Salmonid fish: MEAP-IHNV

The MEAP-IHNV database provides access to detailed data for anyone interested in IHNV molecular epidemiology, such as fish health professionals, fish culture facility managers, and academic researchers. The flexible search capabilities enable the user to generate various output formats, including tables and maps, which should assist users in developing and testing hypotheses about how IHNV moves across landscapes and changes over time. The MEAP-IHNV database is available online at http://gis.nacse.org/ihnv/ (fig. 1). The database contains records that provide background information and genetic sequencing data for more than 1,000 individual field isolates of the fish virus Infectious hematopoietic necrosis virus (IHNV), and is updated approximately annually. It focuses on IHNV isolates collected throughout western North America from 1966 to the present. The database also includes a small number of IHNV isolates from Eastern Russia. By engaging the expertise of the broader community of colleagues interested in IHNV, our goal is to enhance the overall understanding of IHNV epidemiology, including defining sources of disease outbreaks and viral emergence events, identifying virus traffic patterns and potential reservoirs, and understanding how human management of salmonid fish culture affects disease. Ultimately, this knowledge can be used to develop new strategies to reduce the effect of IHN disease in cultured and wild fish.

Fact Sheet↗

USGS2018

Intensive oyster aquaculture can reduce disease impacts on sympatric wild oysters

Risks associated with disease spread from fish and shellfish farming have plagued the growth and public perception of aquaculture worldwide. However, by processing nutrients and organic material from the water column, the culture of many suspension-feeding bivalves has been proposed as a novel solution toward mitigating problems facing coastal water quality, including the removal of disease-causing parasites. Here we developed and simulated an epidemiological model describing sympatric oyster Crassostrea virginica populations in aquaculture and the wild impacted by the protozoan parasite Perkinsus marinus . Our model captured the indirect interaction between wild and cultured populations that occurs through sharing water-borne P. marinus transmission stages, and we hypothesized that oyster aquaculture can enhance wild oyster populations through reduced parasitism as long as cultured oysters are harvested prior to spreading disease. We found that the density of oysters in aquaculture, which is commonly thought to lead to the spread of disease through farms and out to nearby populations in the wild, has only indirect effects on P. marinus transmission through its interaction with the rate of aquaculture harvests. Sufficient aquaculture harvest, which varies with the susceptibility of farmed oysters to P. marinus infection and their lifespan once infected, reduces disease by diluting parasites in the environment. Our modeling results offer new insights toward the broader epidemiological implications of oyster aquaculture and effective disease management.

Aquaculture Environment Interactions↗

USGS2025

A nationwide evaluation of crowd-sourced ambient temperature data

Growing concerns about heat in urban areas paired with the sparsity of weather stations have resulted in individuals drawing on data from citizen science sensor networks to fill in data gaps. The PurpleAir are the most widely-used low-cost air quality sensors in the contiguous United States with 14,777 deployed between 1 Jan 2017 and 20 July 2021. Although the air quality data from PurpleAir sensors have been widely studied, less attention has been paid to reported temperature. We compare temperature metrics reported by PurpleAir sensors with a gridded temperature product, the North American Land Data Assimilation System (NLDAS)-2, which although not a gold-standard measure of temperature, is widely used in epidemiologic research. We evaluate the lag between indoor and outdoor PurpleAir temperatures. We report associations of the difference between outdoor PurpleAir temperatures and NLDAS-2 temperatures, an indicator of degradation, and the duration of sensor operation. Finally, based on the temperature range recorded by the outdoor PurpleAir sensors vis.a.vis NLDAS-2 temperatures, we provide a list of 271 (2.5%) sensors potentially misclassified as outdoor and likely located indoors. We observed that outdoor PurpleAir sensors agreed well with NLDAS-2 (R2 > 0.82). This association broke down under warm conditions (daily average NLDAS ≥ 21.1oC). Landcover and climate zone were significant modifiers of the association between PurpleAir and NLDAS-2 temperature metrics with the poorest PurpleAir- NLDAS-2 agreement in urban areas. Indoor PurpleAir temperatures lagged hourly NLDAS temperatures by two hours across almost all climate zones. The mean difference in hourly PurpleAir and NLDAS-2 temperatures increased by 0.57oC for every operational year, suggesting that careful attention must be paid to degradation. Overall, we find for use in epidemiological studies, that the PurpleAir sensor data is a reliable metric of daytime mean air temperature, but researchers should be aware of its limitations when examining extreme heat, or when aggregating sensor data across multiple years.

Frontiers of Environmental Science and Engineering↗

USGS2020

Eradication of peste des petits ruminants and the wildlife-livestock interface

Growing evidence suggests that multiple wildlife species can be infected with peste des petits ruminants virus (PPRV), with important consequences for the potential maintenance of PPRV in communities of susceptible hosts, and the threat that PPRV may pose to the conservation of wildlife populations and resilience of ecosystems. Significant knowledge gaps in the epidemiology of PPRV across the ruminant community (wildlife and domestic), and the understanding of infection in wildlife and other atypical host species groups (e.g., camelidae, suidae, and bovinae) hinder our ability to apply necessary integrated disease control and management interventions at the wildlife-livestock interface. Similarly, knowledge gaps limit the inclusion of wildlife in the FAO/OIE Global Strategy for the Control and Eradication of PPR, and the framework of activities in the PPR Global Eradication Programme that lays the foundation for eradicating PPR through national and regional efforts. This article reports on the first international meeting on, “Controlling PPR at the livestock-wildlife interface,” held in Rome, Italy, March 27–29, 2019. A large group representing national and international institutions discussed recent advances in our understanding of PPRV in wildlife, identified knowledge gaps and research priorities, and formulated recommendations. The need for a better understanding of PPRV epidemiology at the wildlife-livestock interface to support the integration of wildlife into PPR eradication efforts was highlighted by meeting participants along with the reminder that PPR eradication and wildlife conservation need not be viewed as competing priorities, but instead constitute two requisites of healthy socio-ecological systems.

Frontiers in Veterinary Science↗

USGS2015

U.S. recreational water quality criteria: a vision for the future

This manuscript evaluates the U.S. Recreational Water Quality Criteria (RWQC) of 2012, based upon discussions during a conference held 11–13 March 2013, in Honolulu, Hawaii. The RWQC of 2012 did not meet expectations among the research community because key recommended studies were not completed, new data to assess risks to bathers exposed to non-point sources of fecal indicator bacteria (FIB) were not developed, and the 2012 RWQC did not show marked improvements in strategies for assessing health risks for bathers using all types of recreational waters. The development of the 2012 RWQC was limited in scope because the epidemiologic studies at beach sites were restricted to beaches with point sources of pollution and water samples were monitored for only enterococci. The vision for the future is development of effective RWQC guidelines based on epidemiologic and quantitative microbial risk assessment (QMRA) studies for sewage specific markers, as well as human enteric pathogens so that health risks for bathers at all recreational waters can be determined. The 2012 RWQC introduced a program for states and tribes to develop site-specific water quality criteria, and in theory this approach can be used to address the limitations associated with the measurements of the traditional FIB.

International Journal of Environmental Research an↗

USGS2010

Model-based evaluation of highly and low pathogenic avian influenza dynamics in wild birds

There is growing interest in avian influenza (AI) epidemiology to predict disease risk in wild and domestic birds, and prevent transmission to humans. However, understanding the epidemic dynamics of highly pathogenic (HPAI) viruses remains challenging because they have rarely been detected in wild birds. We used modeling to integrate available scientific information from laboratory and field studies, evaluate AI dynamics in individual hosts and waterfowl populations, and identify key areas for future research. We developed a Susceptible-Exposed-Infectious-Recovered (SEIR) model and used published laboratory challenge studies to estimate epidemiological parameters (rate of infection, latency period, recovery and mortality rates), considering the importance of age classes, and virus pathogenicity. Infectious contact leads to infection and virus shedding within 1–2 days, followed by relatively slower period for recovery or mortality. We found a shorter infectious period for HPAI than low pathogenic (LP) AI, which may explain that HPAI has been much harder to detect than LPAI during surveillance programs. Our model predicted a rapid LPAI epidemic curve, with a median duration of infection of 50–60 days and no fatalities. In contrast, HPAI dynamics had lower prevalence and higher mortality, especially in young birds. Based on field data from LPAI studies, our model suggests to increase surveillance for HPAI in post-breeding areas, because the presence of immunologically naïve young birds is predicted to cause higher HPAI prevalence and bird losses during this season. Our results indicate a better understanding of the transmission, infection, and immunity-related processes is required to refine predictions of AI risk and spread, improve surveillance for HPAI in wild birds, and develop disease control strategies to reduce potential transmission to domestic birds and/or humans.

PLoS ONE↗

USGS2013

Animal migration and risk of spread of viral infections

The potential contribution of migration towards the spread of disease is as varied as the ecology of the pathogens themselves and their host populations. This chapter outlines multiple examples of viral diseases in animal populations and their mechanisms of viral spread. Many species of insects, mammals, fish, and birds exhibit migratory behavior and have the potential to disperse diseases over long distances. The majority of studies available on viral zoonoses have focused on birds and bats, due to their highly migratory life histories. A number of studies have reported evidence of changes in the timing of animal migrations in response to climate change. The majority indicate an advancement of spring migration, with few or inconclusive results for fall migration. Predicting the combined effects of climate change on migratory patterns of host species and epidemiology of viral pathogens is complex and not fully realistic.

Book chapter↗

USGS2019

Simultaneous autoregressive (SAR) model

Simultaneous autoregressive (SAR) models are useful for accommodating various forms of dependence among data that have discrete support in a space of interest. These models are often specified hierarchically as mixed-effects regression models with first-moment structure controlled by a conventional linear regression term and second-moment structure induced by correlated random effects. In their general form, SAR models resemble conditional autoregressive (CAR) models, and can be made equivalent but are often parameterized differently. Importantly, SAR models can be specified by simultaneously regressing a discrete spatial process on itself. Thus, they allow one to construct statistical models for processes with directional graphical properties that pertain to data generating mechanisms. Most commonly SAR models have been used to account for structure among data with areal spatial support in applications involving ecology, epidemiology, sociology, and environmental science.

Book chapter↗

USGS2017

Transmission routes maintaining a viral pathogen of steelhead trout within a complex multi-host assemblage

This is the first comprehensive region wide, spatially explicit epidemiologic analysis of surveillance data of the aquatic viral pathogen infectious hematopoietic necrosis virus (IHNV) infecting native salmonid fish. The pathogen has been documented in the freshwater ecosystem of the Pacific Northwest of North America since the 1950s, and the current report describes the disease ecology of IHNV during 2000–2012. Prevalence of IHNV infection in monitored salmonid host cohorts ranged from 8% to 30%, with the highest levels observed in juvenile steelhead trout. The spatial distribution of all IHNV-infected cohorts was concentrated in two sub-regions of the study area, where historic burden of the viral disease has been high. During the study period, prevalence levels fluctuated with a temporal peak in 2002. Virologic and genetic surveillance data were analyzed for evidence of three separate but not mutually exclusive transmission routes hypothesized to be maintaining IHNV in the freshwater ecosystem. Transmission between year classes of juvenile fish at individual sites (route 1) was supported at varying levels of certainty in 10%–55% of candidate cases, transmission between neighboring juvenile cohorts (route 2) was supported in 31%–78% of candidate cases, and transmission from adult fish returning to the same site as an infected juvenile cohort was supported in 26%–74% of candidate cases. The results of this study indicate that multiple specific transmission routes are acting to maintain IHNV in juvenile fish, providing concrete evidence that can be used to improve resource management. Furthermore, these results demonstrate that more sophisticated analysis of available spatio-temporal and genetic data is likely to yield greater insight in future studies.

Idaho, Oregon, Washington↗

USGS2023

Spatial modeling of two mosquito vectors of West Nile virus using integrated nested Laplace approximations

The abundance of Culex restuans and Culex pipiens in relation to ecological predictors is poorly understood in regions of the United States where their ranges overlap. It is suspected that these species play different roles in spreading West Nile virus (WNV) in these regions, but few studies have modeled these species separately or accounted for spatial correlation using Bayesian methods. We used mosquito surveillance data collected by the Pennsylvania Department of Environmental Protection from 2002 to 2016 and integrated nested Laplace approximations with the stochastic partial differential equation approach to predict C. restuans and C. pipiens abundance in relation to several ecological predictors. We then made a predictive risk surface of abundance for each species at locations that were not sampled. Explanatory variables in the models included ecological variables previously described to be important predictors of the abundance of these mosquito species. Developed habitat, temperature, and precipitation were important predictor variables for the abundance of C. restuans , whereas developed habitat, snow water equivalent, and normalized difference water index were important predictor variables for the abundance of C. pipiens . The abundance of C. restuans had a negative relationship with developed habitat in contrast to C. pipiens abundance, which had a positive relationship with developed habitat. Julian date was modeled as a temporal trend for both species and showed C. restuans to be more abundant from late April through late June and C. pipiens to be more abundant from July through September. A seasonal crossover was observed between these two species on Julian day 185, 4 July. We observed different spatial patterns of abundance in the predictive risk maps of each of the species. Our results indicate that modeling the abundance of these species spatially and separately in regions where these two mosquito vectors coexist can help gain further insight into understanding the epidemiology of WNV in human and susceptible animal populations.

Pennsylvania↗

USGS2016

Chronic wasting disease in white-tailed deer: Infection, mortality, and implications for heterogeneous transmission

Chronic wasting disease (CWD) is a fatal neurodegenerative disease affecting free-ranging and captive cervids that now occurs in 24 U.S. states and two Canadian provinces. Despite the potential threat of CWD to deer populations, little is known about the rates of infection and mortality caused by this disease. We used epidemiological models to estimate the force of infection and disease-associated mortality for white-tailed deer in the Wisconsin and Illinois CWD outbreaks. Models were based on age-prevalence data corrected for bias in aging deer using the tooth wear and replacement method. Both male and female deer in the Illinois outbreak had higher corrected age-specific prevalence with slightly higher female infection than deer in the Wisconsin outbreak. Corrected ages produced more complex models with different infection and mortality parameters than those based on apparent prevalence. We found that adult male deer have a more than threefold higher risk of CWD infection than female deer. Males also had higher disease mortality than female deer. As a result, CWD prevalence was twofold higher in adult males than females. We also evaluated the potential impacts of alternative contact structures on transmission dynamics in Wisconsin deer. Results suggested that transmission of CWD among male deer during the nonbreeding season may be a potential mechanism for producing higher rates of infection and prevalence characteristically found in males. However, alternatives based on high environmental transmission and transmission from females to males during the breeding season may also play a role.

Ecology↗

USGS2017

Infectious hematopoietic necrosis virus virological and genetic surveillance 2000–2012

Surveillance records of the acute RNA pathogen of Pacific salmonid fish infectious hematopoietic necrosis virus are combined for the first time to enable landscape-level ecological analyses and modeling. The study area is the freshwater ecosystems of the large Columbia River watershed in the U.S. states of Washington, Oregon, and Idaho, as well as coastal rivers in Washington and Oregon. The study period is 2000–2012, and records were contributed by all five resource management agencies that operate conservation hatcheries in the study area. Additional records from wild fish were collected from the National Wild Fish Health Survey, operated by the U.S. Fish and Wildlife Survey. After curation and normalization, the data set consists of 6766 records, representing 1146 sample sites and 15 different fish hosts. The virus was found in an average of 12.4% of records, and of these 66.2% also have viral genetic analysis available. This data set is used to conduct univariate ecological and epidemiological analyses and develop a novel hierarchical landscape transmission model for an aquatic pathogen.

Ecology↗

USGS2020

Trait‐based variation in host contribution to pathogen transmission across species and resource supplies

Two key knowledge gaps currently limit the development of more predictive and general models of pathogen transmission: (1) the physiological basis of heterogeneity in host contribution to pathogen transmission (reservoir potential) remains poorly understood, and (2) a general means of integrating the ecological dynamics of host communities has yet to emerge. If the traits responsible for differences in reservoir potential also modulate host community dynamics, these traits could be used to predict pathogen transmission as host communities change. In two greenhouse experiments, across 23 host species and two levels of resource supply, the reservoir potential of plant hosts increased significantly along the Leaf Economic Spectrum, a global axis of plant physiological trait covariation that features prominently in models of plant community ecology. This indicates that the traits of the Leaf Economic Spectrum underlie broad differences in reservoir potential across host species and resource supplies. Therefore, host traits could be used to integrate epidemiological models of pathogen transmission with ecological models of host community change.

Ecology↗