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Disease‐structured N‐mixture models: A practical guide to model disease dynamics using count data

Obtaining inferences on disease dynamics (e.g., host population size, pathogen prevalence, transmission rate, host survival probability) typically requires marking and tracking individuals over time. While multistate mark–recapture models can produce high‐quality inference, these techniques are difficult to employ at large spatial and long temporal scales or in small remnant host populations decimated by virulent pathogens, where low recapture rates may preclude the use of mark–recapture techniques. Recently developed N ‐mixture models offer a statistical framework for estimating wildlife disease dynamics from count data. N ‐mixture models are a type of state‐space model in which observation error is attributed to failing to detect some individuals when they are present (i.e., false negatives). The analysis approach uses repeated surveys of sites over a period of population closure to estimate detection probability. We review the challenges of modeling disease dynamics and describe how N ‐mixture models can be used to estimate common metrics, including pathogen prevalence, transmission, and recovery rates while accounting for imperfect host and pathogen detection. We also offer a perspective on future research directions at the intersection of quantitative and disease ecology, including the estimation of false positives in pathogen presence, spatially explicit disease‐structured N ‐mixture models, and the integration of other data types with count data to inform disease dynamics. Managers rely on accurate and precise estimates of disease dynamics to develop strategies to mitigate pathogen impacts on host populations. At a time when pathogens pose one of the greatest threats to biodiversity, statistical methods that lead to robust inferences on host populations are critically needed for rapid, rather than incremental, assessments of the impacts of emerging infectious diseases.

Ecology and Evolution

Pneumonia in bighorn sheep: Risk and resilience

Infectious disease was an important driver of historic declines and extirpations of bighorn sheep (Ovis canadensis) in North America and continues to impede population restoration and management. Domestic sheep have long been linked to pneumonia outbreaks in bighorn sheep and this association has now been confirmed in 13 captive commingling experiments. However, ecological and etiological complexities still hinder our understanding and control of the disease. We provide an overview of the current state of knowledge about the biology and management of respiratory disease in bighorn sheep and propose strategies for moving forward. Epizootic pneumonia in bighorn sheep is polymicrobial. Mycoplasma ovipneumoniae, a bacterium host-specific to Caprinae and commonly carried by healthy domestic sheep and goats appears to be a necessary primary agent. All-age epizootics following introduction of M. ovipneumoniae along with other pathogens into bighorn sheep populations are usually severe (median mortality 47%) but fatality rates vary widely, from 15 – 100%. Disease severity may be influenced by the strain of M. ovipneumoniae, by secondary bacterial and viral pathogens, and by factors affecting transmission and host immunity. Once introduced, M. ovipneumoniae can persist in bighorn sheep populations for decades. Carrier dams transmit the pathogen to their susceptible lambs, triggering fatal pneumonia outbreaks in nursery groups, which limits recruitment and slows or prevents population recovery. The result is that demographic costs of pathogen persistence often outweigh the impacts of the initial invasion and die-off. There is currently no effective vaccine or antibiotic for domestic or wild sheep and to date, no management actions have been successful in reducing morbidity, mortality, or disease spread once pathogen invasion has occurred. Molecular-based strain typing suggests that spillover of M. ovipneumoniae into bighorn sheep populations from domestic small ruminants is ongoing, and that consequences of pathogen invasion are amplified by movements of infected bighorn sheep. Therefore, current disease management strategies focus on reducing risk of spillover from reservoir populations of domestic small ruminants and on limiting transmission among bighorn sheep. A broad array of approaches has been tried and more are needed to prevent pathogen introduction, induce disease fadeout in persistently infected populations, and promote population resilience across the diverse landscapes bighorn sheep inhabit. A comprehensive examination of disease dynamics across populations could help elucidate how disease fades out naturally and if population resilience can be increased in the face of infection. Cross-jurisdictional adaptive management experiments and transdisciplinary collaboration, including partnerships with members of the domestic sheep and goat community, are needed to facilitate innovation and speed progress towards sustainable solutions for managing pneumonia to protect and restore bighorn sheep populations.

California, Idaho, Nevada, Oregon, Utah, Washingto

Statewide quantitative microbial risk assessment for waterborne viruses, bacteria, and protozoa in public water supply wells in Minnesota

Infection risk from waterborne pathogens can be estimated via quantitative microbial risk assessment (QMRA) and forms an important consideration in the management of public groundwater systems. However, few groundwater QMRAs use site-specific hazard identification and exposure assessment, so prevailing risks in these systems remain poorly defined. We estimated the infection risk for 9 waterborne pathogens based on a 2-year pathogen occurrence study in which 964 water samples were collected from 145 public wells throughout Minnesota, USA. Annual risk across all nine pathogens combined was 3.3 × 10 –1 (95% CI: 2.3 × 10 –1 to 4.2 × 10 –1 ), 3.9 × 10 –2 (2.3 × 10 –2 to 5.4 × 10 –2 ), and 1.2 × 10 –1 (2.6 × 10 –2 to 2.7 × 10 –1 ) infections person –1 year –1 for noncommunity, nondisinfecting community, and disinfecting community wells, respectively. Risk estimates exceeded the U.S. benchmark of 10 –4 infections person –1 year –1 in 59% of well-years, indicating that the risk was widespread. While the annual risk for all pathogens combined was relatively high, the average daily doses for individual pathogens were low, indicating that significant risk results from sporadic pathogen exposure. Cryptosporidium dominated annual risk, so improved identification of wells susceptible to Cryptosporidium contamination may be important for risk mitigation.

Minnesota

Diverse novel and avian-associated viruses in the ileal viromes of northern mockingbird (Mimus polyglottos)

Viruses are the most abundant and diverse organisms on Earth, though only a small portion cause disease. Understanding viral diversity is key to understanding and predicting pathogen emergence and zoonotic spillover. Here, we use meta-transcriptomic sequencing to examine the viral communities in the ileum of 25 Northern Mockingbirds ( Mimus polyglottos ) from various locations across Texas. We assembled high-quality genomes of 43 viral species (40 species identified to 13 families, one to kingdom, and two to realm), 38 of which were novel. They tentatively represent avian- (n = 3), arthropod- (n = 21), plant- (n = 5) and fungi- (n = 4) associated, or other (n = 10) viruses. The arthropod-associated Dicistroviridae family was the most dominant, comprising known and potentially new species. Of potential epidemiological importance were three novel and avian-associated viruses: members of the families Hepeviridae and Picornaviridae , and a new Matryoshka RNA virus. The Matryoshka RNA virus 8 (MaRNAV-8) is sister to other Matryoshka RNA viruses, and its co-occurrence with haemosporida further supports the nested virus-parasite-vector-vertebrate host relationship of this group of viruses, with potential implications for parasite evolution, fitness and load and vector competence. The Picornaviridae virus is a member of an avian hepatovirus clade, found nested within a clade containing both the mammalian pathogens Hepatovirus A – I and the avian Tremovirus pathogens, suggestive of a newly discovered pathogen of Northern Mockingbird. Although the recovered Hepeviridae virus is of unknown pathology, its family members include the Hepatitis E viruses. With the great diversity and novelty described from ileal viromes, discriminating potential pathogens and commensal microbiota from viruses associated with food items remains challenging. A deeper understanding of virus transmission and the risk of potential zoonosis can be enhanced by tracking viruses through the food web and via inter-specific and predator-prey interactions, particular in areas subject to land-use change, where human-wildlife interactions are increased and the risks from emerging pathogens of veterinary and medical importance are more pronounced.

Texas

Geographic setting influences Great Lakes beach microbiological water quality

Understanding of factors that influence Escherichia coli (EC) and enterococci (ENT) concentrations, pathogen occurrence, and microbial sources at Great Lakes beaches comes largely from individual beach studies. Using 12 representative beaches, we tested enrichment cultures from 273 beach water and 22 tributary samples for EC, ENT, and genes indicating the bacterial pathogens Shiga-toxin producing E. coli (STEC), Shigella spp., Salmonella spp, Campylobacter jejuni/coli, and methicillin-resistant Staphylococcus aureus, and 108–145 samples for Bacteroides human, ruminant, and gull source-marker genes. EC/ENT temporal patterns, general Bacteroides concentration, and pathogen types and occurrence were regionally consistent (up to 40 km), but beach catchment variables (drains/creeks, impervious surface, urban land cover) influenced exceedances of EC/ENT standards and detections of Salmonella and STEC. Pathogen detections were more numerous when the EC/ENT Beach Action Value (but not when the Geometric Mean and Statistical Threshold Value) was exceeded. EC, ENT, and pathogens were not necessarily influenced by the same variables. Multiple Bacteroides sources, varying by date, occurred at every beach. Study of multiple beaches in different geographic settings provided new insights on the contrasting influences of regional and local variables, and a broader-scale perspective, on significance of EC/ENT exceedances, bacterial sources, and pathogen occurrence.

Great Lakes

Cross-species transmission potential between wild pigs, livestock, poultry, wildlife, and humans: Implications for disease risk management in North America

Cross-species disease transmission between wildlife, domestic animals and humans is an increasing threat to public and veterinary health. Wild pigs are increasingly a potential veterinary and public health threat. Here we investigate 84 pathogens and the host species most at risk for transmission with wild pigs using a network approach. We assess the risk to agricultural and human health by evaluating the status of these pathogens and the co-occurrence of wild pigs, agriculture and humans. We identified 34 (87%) OIE listed swine pathogens that cause clinical disease in livestock, poultry, wildlife, and humans. On average 73% of bacterial, 39% of viral, and 63% of parasitic pathogens caused clinical disease in other species. Non-porcine livestock in the family Bovidae shared the most pathogens with swine (82%). Only 49% of currently listed OIE domestic swine diseases had published wild pig surveillance studies. The co-occurrence of wild pigs and farms increased annually at a rate of 1.2% with as much as 57% of all farms and 77% of all agricultural animals co-occurring with wild pigs. The increasing co-occurrence of wild pigs with livestock and humans along with the large number of pathogens shared is a growing risk for cross-species transmission.

Scientific Reports

Island of misfit tortoises: Waif gopher tortoise health assessment following translocation

Translocation, the intentional movement of animals from one location to another, is a common management practice for the gopher tortoise ( Gopherus polyphemus ). Although the inadvertent spread of pathogens is a concern with any translocation effort, waif tortoises—individuals that have been collected illegally, injured and rehabilitated or have unknown origins—are generally excluded from translocation efforts due to heightened concerns of introducing pathogens and subsequent disease to naïve populations. However, repurposing these long-lived animals for species recovery is desirable when feasible, and introducing waif tortoises may bolster small populations facing extirpation. The objective of this study was to assess the health of waif tortoises experimentally released at an isolated preserve in Aiken County, SC, USA. Our assessments included visual examination, screening for 14 pathogens using conventional or quantitative polymerase chain reaction (qPCR) and haematological evaluation. Of the 143 individuals assessed in 2017 and 2018, most individuals (76%; n = 109 of 143) had no overt clinical evidence of disease and, when observed, clinical findings were mild. In both years, we detected two known tortoise pathogens, Mycoplasma agassizii and Mycoplasma testudineum , at a prevalence of 10.2–13.9% and 0.0–0.8%, respectively. Additionally, we found emydid Mycoplasma , a bacterium commonly found in box turtles ( Terrapene spp . ), in a single tortoise that showed no clinical evidence of infection. The presence of nasal discharge was an important, but imperfect, predictor of Mycoplasma spp. infection in translocated tortoises. Hemogram data were comparable with wild populations. Our study is the first comprehensive effort to assess pathogen prevalence and hemogram data of waif gopher tortoises following translocation. Although caution is warranted and pathogen screening necessary, waif tortoises may be an important resource for establishing or augmenting isolated populations when potential health risks can be managed.

Conservation Physiology

Variation in within-host replication kinetics among virus genotypes provides evidence of specialist and generalist infection strategies across three salmonid host species

Theory of the evolution of pathogen specialization suggests that a specialist pathogen gains high fitness in one host, but this comes with fitness loss in other hosts. By contrast, a generalist pathogen does not achieve high fitness in any host, but gains ecological fitness by exploiting different hosts, and has higher fitness than specialists in nonspecialized hosts. As a result, specialist pathogens are predicted to have greater variation in fitness across hosts, and generalists would have lower fitness variation across hosts. We test these hypotheses by measuring pathogen replicative fitness as within-host viral loads from the onset of infection to the beginning of virus clearance, using the rhabdovirus infectious hematopoietic necrosis virus (IHNV) in salmonid fish. Based on field prevalence and virulence studies, the IHNV subgroups UP, MD, and L are specialists, causing infection and mortality in sockeye salmon, steelhead, and Chinook salmon juveniles, respectively. The UC subgroup evolved naturally from a UP ancestor and is a generalist infecting all three host species but without causing severe disease. We show that the specialist subgroups had the highest peak and mean viral loads in the hosts in which they are specialized, and they had low viral loads in nonspecialized hosts, resulting in large variation in viral load across hosts. Viral kinetics show that the mechanisms of specialization involve the ability to both maximize early virus replication and avoid clearance at later times, with different mechanisms of specialization evident in different host–virus combinations. Additional nuances in the data included different fitness levels for nonspecialist interactions, reflecting different trade-offs for specialist viruses in other hosts. The generalist UC subgroup reached intermediate viral loads in all hosts and showed the smallest variation in fitness across hosts. The evolution of the UC generalist from an ancestral UP sockeye specialist was associated with fitness increases in steelhead and Chinook salmon, but only slight decreases in fitness in sockeye salmon, consistent with low- or no-cost generalism. Our results support major elements of the specialist–generalist theory, providing evidence of a specialist–generalist continuum in a vertebrate pathogen. These results also quantify within-host replicative fitness trade-offs resulting from the natural evolution of specialist and generalist virus lineages in multi-host ecosystems

Virus Evolution

Stochastic within-host dynamics and climate-sensitive traits generate predictable patterns of variation in disease outcomes

Understanding how climatic variables impact host-pathogen relationships in temperature-sensitive ectothermic host organisms is crucial under global change. Few studies have explored how temperature gradients generate inter-individual variation in epidemiological traits like host susceptibility or pathogen replication. Here, we develop a mathematical model to explore a novel hypothesis: stochastic within-host dynamics and simulated thermal mismatches between host and pathogen traits generate predictable variation in infection outcomes among hosts and across thermal gradients. Our model demonstrates that varying trait thermal optima in host immunity and pathogen replication, and stochastic within-host processes produced variation in infection outcomes. Variability was low when temperatures strongly favored host or pathogen traits, but high and diverse when their performance was similar across a broad thermal range. In contrast, when trait performance was equal across all temperatures (no mismatch) variability remained low at all temperatures. Further, the magnitude of variation, quantified by entropy, exhibited predictable patterns depending on host-pathogen thermal mismatches. We conclude that interactions between trait thermal mismatches and within-host stochasticity provide a theoretical framework to improve ectotherm disease models under climate change, providing a valuable tool for exploring the impacts of environmental change on epizootic or epidemic dynamics, particularly in vulnerable marine ecosystems.

Philosophical Transactions of the Royal Society, S

Quantitative support for the benefits of proactive management for wildlife disease control

Finding effective pathogen mitigation strategies is one of the biggest challenges humans face today. In the context of wildlife, emerging infectious diseases have repeatedly caused widespread host morbidity and population declines of numerous taxa. In areas yet unaffected by a pathogen, a proactive management approach has the potential to minimize or prevent host mortality. However, typically critical information on disease dynamics in a novel host system is lacking, empirical evidence on efficacy of management interventions is limited, and there is a lack of validated predictive models. As such, quantitative support for identifying effective management interventions is largely absent, and the opportunity for proactive management is often missed. We considered the potential invasion of the chytrid fungus, Batrachochytrium salamandrivorans (Bsal), whose expected emergence in North America poses a severe threat to hundreds of salamander species in this global salamander biodiversity hotspot. We developed and parameterized a dynamic multistate occupancy model to forecast host and pathogen occurrence, following expected emergence of the pathogen, and evaluated the response of salamander populations to different management scenarios. Our model forecasted that taking no action is expected to be catastrophic to salamander populations. Proactive action was predicted to maximize host occupancy outcomes relative to wait-and-see reactive management, thus providing quantitative support for proactive management opportunities. The eradication of Bsal was unlikely under all the evaluated management options. Contrary to our expectations, even early pathogen detection had little effect on Bsal or host occupancy outcomes. Our results provide quantitative support that proactive management is the optimal strategy for promoting persistence of disease-threatened salamander populations. Our approach fills a critical gap by defining a framework for evaluating management options prior to pathogen invasion and can thus serve as a template for addressing novel disease threats that jeopardize wildlife and human health.

Conservation Biology

Climate warming and disease risks for terrestrial and marine biota

Infectious diseases can cause rapid population declines or species extinctions. Many pathogens of terrestrial and marine taxa are sensitive to temperature, rainfall, and humidity, creating synergisms that could affect biodiversity. Climate warming can increase pathogen development and survival rates, disease transmission, and host susceptibility. Although most host-parasite systems are predicted to experience more frequent or severe disease impacts with warming, a subset of pathogens might decline with warming, releasing hosts from disease. Recently, changes in El Niño–Southern Oscillation events have had a detectable influence on marine and terrestrial pathogens, including coral diseases, oyster pathogens, crop pathogens, Rift Valley fever, and human cholera. To improve our ability to predict epidemics in wild populations, it will be necessary to separate the independent and interactive effects of multiple climate drivers on disease impact.

Science

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

Leveraging detection uncertainty to estimate Renibacterium salmoninarum infection status among multiple tissues and assays

Effective disease surveillance relies on accurate pathogen testing and robust prevalence estimates. Diagnostic specificity (DSp), the probability that an uninfected animal tests negative, is high when false positives are low. Diagnostic sensitivity (DSe) is the probability an infected animal tests positive; higher DSe means fewer false negatives. However, sensitivity and false negatives are harder to estimate without a "gold standard", an assay that can detect between 90 - 100% of true positive infections. Occupancy estimation of infection prevalence offers one solution by allowing for imperfect detection of the pathogen. Testing potentially infected tissues multiple times allows for the use of a Bayesian multistate occupancy model to estimate the probability of pathogen infection in tissues [Formula: see text] and detection probabilities [Formula: see text] for different assays. Using [Formula: see text] and [Formula: see text] from the posterior distribution, the conditional probability of detecting the pathogen can be modeled, allowing for the calculation of DSe. Renibacterium salmoninarum is a bacterial pathogen causing bacterial kidney disease among salmonid species and was the model pathogen we used to train our model. The current testing standard for salmonids combines initial screening for antibodies using direct fluorescent antibody test (DFAT) with polymerase chain reaction (PCR) confirmation to detect R. salmoninarum. However, detection of R. salmoninarum still varies between species, tissues, and assays. Here, a multi-state occupancy model was used to estimate detection probability among individual and dual kidney/liver infections with DFAT and qPCR in fish with an unknown infection status. Both assays produced false negatives, but qPCR had fewer than DFAT and a higher DSe. Infection state was often misclassified, but multiple surveys per individual or combining tissues for testing improved DSe for both assays.

conterminous United States

Risk assessment for the reintroduction of anadromous salmonids upstream of Chief Joseph and Grand Coulee Dams, Northeastern Washington

The Upper Columbia United Tribes (UCUT; Spokane, Colville, Kootenai, Coeur d’Alene, and Kalispel Tribes) and Washington Department of Fish and Wildlife want to reintroduce anadromous salmonids to their historical range to restore ecosystem function and lost cultural and spiritual relationships in the upper Columbia River, northeastern Washington. The UCUT contracted with the U.S. Geological Survey to assess risks to resident taxa (existing fish populations in the reintroduction area upstream of Chief Joseph and Grand Coulee Dams) and reintroduced salmon associated with reintroduction. We developed a risk assessment framework for reintroduction of anadromous salmonids upstream of Chief Joseph and Grand Coulee Dams. To accomplish this goal, we applied strategies identified in previous risk assessment frameworks for reintroduction. The risk assessment is an initial step towards an anadromous reintroduction strategy. An initial list of potential donor sources for reintroduction species was developed from previous published sources for Chinook Salmon ( Oncorhynchus tshawytscha ) donors in the Transboundary Reach of the Columbia River, British Columbia; an ecological risk assessment of upper Columbia River hatchery programs on non-target taxa of concern; and a review of existing hatchery programs During two workshops, we further identified and ranked potential donor sources of anadromous Redband Trout (steelhead; O. mykiss ), Chinook Salmon, Sockeye Salmon ( O. nerka ), and Coho Salmon ( O. kisutch ). We also identified resident fish populations of interest and their primary habitat, location, status, and pathogen concerns to determine the potential risks of reintroduction. Species were deemed of interest based on resource management and potential interactions (that is, genetics, competition, and predation) with introduced species. We developed tables of potential donors by species and characterized potential sources (hatchery and natural origins), populations (individual runs), broodstock management and history, and potential constraints (that is, Endangered Species Act [ESA] listing, Evolutionarily Significant Unit concerns, pathogens, and availability). During the workshops, a group of regional fisheries and topic experts subjectively ranked the relative risks of pathogens, genetic effects, predation, and competition to resident fish and reintroduced salmonids. We assessed the pathogen risk of each potential donor for introducing new pathogens and the increased burden to existing pathogens for resident species upstream of the dams. We considered genetic risks to resident and downstream conspecifics and ecological impacts, including competition for food and space, predator-prey interactions, and ecosystem benefits/impacts. Each reintroduced species donor source was ranked based on abundance/viability (demographic risk to source and feasibility of collection), ancestral/genetic similarity (evolutionary similarity to historical populations), local adaptation (geographic proximity/similarity of source conditions to reintroduction conditions), and life history compatibility (including migration; spawn timing; and relative usage of reservoir, main-stem, or tributary habitats) with environmental conditions in the reintroduction area. We synthesized this information by species for all potential donors, in which an overall score and ranking system was established for decision support in donor selection for reintroduction into the upper Columbia River. We also provided information outside the ranking process by: Identifying predator-prey interactions and competition for food and space among species, Developing a decision support framework for donor selection, and Providing decision support for reintroduction strategies.

Washington

Identification of bacteria in groundwater used for domestic supply in the southeast San Joaquin Valley, California, 2014

Groundwater is an important source of drinking water in California. Water-borne diseases caused by microbial contamination are a growing concern. The MI test, a membrane filtration method for the chromogenic/fluorogenic detection of total coliforms and Escherichia coli , was used for samples collected January to April 2014 from 42 domestic wells in the southeastern San Joaquin Valley. The wells were sampled as part of the Groundwater Ambient Monitoring and Assessment Program Priority Basin Project (GAMA-PBP), a cooperative study between the U.S. Geological Survey and the California State Water Resources Control Board. Polymerase chain reaction analysis and sequencing of deoxyribonucleic acid (DNA) were used for 34 target and nontarget colonies that grew on the MI media from samples collected from 13 of the domestic wells to identify what genera of bacteria could exist in groundwater used by domestic wells. Gene sequences obtained using the Sanger method were entered into the basic local alignment search tool (BLAST) database, and 17 genera of bacteria were identified. Of these, 13 genera contain species that are human pathogens or opportunistic human pathogens. All the genera that include human pathogens are naturally present in soil, plants, or water; one of the pathogens also can be found in fecal matter. Six of the human pathogens were from non-target colony growth on the MI media. Target and non-target microbial growth on MI media are indicators of the possible presence of pathogenic bacteria even if the bacteria naturally are from soil rather than from a fecal source.

California

Keeping the heat on: Weighted surveillance for Chytrid fungus (Batrachochytirum dendrobatidis) in Dixie Valley toads (Anaxyrus [= Bufo] williamsi)

Introduced fungal pathogens have caused declines and extinctions of naïve wildlife populations across vertebrate classes. Consequences of introduced pathogens to hosts with small ranges might be especially severe because of limited redundancy to rescue populations and lower abundance that may limit the resilience of populations to perturbations like disease introduction. As a complement to biosecurity measures to prevent the spread of pathogens, surveillance programs may enable early detection of pathogens, when management actions to limit the effects of pathogens on naïve hosts might be most beneficial. We analyzed surveillance data for the endangered and narrowly endemic Dixie Valley toad ( Anaxyrus [= Bufo ] williamsi ) from two time periods (2011–2014 and 2019–2021) to estimate the minimum detectable prevalence of the amphibian fungal pathogen Batrachochytrium dendrobatidis ( Bd ). We assessed if detection efficiency could be improved by using samples from both Dixie Valley toads and co-occurring introduced American bullfrogs ( Lithobates catesbeianus ) and literature-derived surveillance weights. We further evaluated a weighted surveillance design to increase the efficiency of surveillance efforts for Bd within the toad’s small (<6 km 2 ) range. We found that monitoring adult and larval American bullfrogs would probably detect Bd more efficiently than monitoring Dixie Valley toads alone. Given that no Bd was detected, minimum detectable prevalence of Bd was <3% in 2011–2014, and <5% (Dixie Valley toads only) and <10% (American bullfrogs only) in 2019–2021. Optimal management for Bd depends on the mechanisms underlying its apparent absence from the range of Dixie Valley toads, but a balanced surveillance scheme that includes sampling American bullfrogs to increase the likelihood of detecting Bd , and adult Dixie Valley toads to ensure broad spatial coverage where American bullfrogs do not occur, would probably result in efficient surveillance, which might permit timely management of Bd if it is detected.

Journal of Wildlife Diseases

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 &ldquo;it is time to close the book on infectious diseases and the war against pestilence won,&rdquo; 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 &ldquo;spillover&rdquo; of human diseases to great ape populations (K&ouml;ndgen 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 &ldquo;villains&rdquo; or reservoirs as well as &ldquo;victims&rdquo; 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

Widespread Ranavirus and Perkinsea infections in Cuban treefrogs (Osteopilus septentrionalis) invading New Orleans, USA

Invasive species can negatively impact ecosystems in numerous ways, including vectoring pathogenic organisms. In amphibians, a lineage globally threatened by multiple pathogens, this spread of disease via invasive species could contribute to declines in native populations. The Cuban Treefrog (Osteopilus septentrionalis) is invasive in the southeastern USA. To assess whether O. septentrionalis is a potential reservoir host for the pathogens Batrachochytrium dendrobatidis (Bd; Amphibian Chytrid Fungus), Ranavirus (Rv), and Perkinsea (Pr), we sampled 82 individuals from a recently invaded site in New Orleans, Louisiana, USA. We used quantitative PCR to assess prevalence and intensity of Bd, Rv, and Pr in mouthparts and tail clips from 22 larvae and in toe clips from 60 metamorphosed frogs. We compared infection prevalence and intensity across host characteristics, including Fulton’s Body Condition, sex, and life stage. None of the individuals were infected with Bd, 72% were infected with Rv, and 44% were infected with Pr. Twenty-three individuals (28%) were co-infected with Rv and Pr, but co-infection did not significantly predict the prevalence or intensity of either Rv or Pr. Although we did not observe any disease signs, Pr infections were significantly associated with lower body condition, suggesting sub-lethal fitness costs. Our study establishes that invasive O. septentrionalis in New Orleans are infected with two pathogens of global concern for amphibians. Understanding host-pathogen dynamics in O. septentrionalis in Louisiana is a critical step towards understanding how this invasive species could threaten amphibian biodiversity in the region by transmitting infectious pathogens.

Louisiana