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USGS2013

Pathophysiology of white-nose syndrome in bats: A mechanistic model linking wing damage to mortality

White-nose syndrome is devastating North American bat populations but we lack basic information on disease mechanisms. Altered blood physiology owing to epidermal invasion by the fungal pathogen Geomyces destructans ( Gd ) has been hypothesized as a cause of disrupted torpor patterns of affected hibernating bats, leading to mortality. Here, we present data on blood electrolyte concentration, haematology and acid–base balance of hibernating little brown bats, Myotis lucifugus , following experimental inoculation with Gd . Compared with controls, infected bats showed electrolyte depletion (i.e. lower plasma sodium), changes in haematology (i.e. increased haematocrit and decreased glucose) and disrupted acid–base balance (i.e. lower CO 2 partial pressure and bicarbonate). These findings indicate hypotonic dehydration, hypovolaemia and metabolic acidosis. We propose a mechanistic model linking tissue damage to altered homeostasis and morbidity/mortality.

Biology Letters↗

USGS2022

Social effects of rabies infection in male vampire bats (Desmodus rotundus)

Rabies virus (RABV) transmitted by the common vampire bat ( Desmodus rotundus ) poses a threat to agricultural development and public health throughout the Neotropics. The ecology and evolution of rabies host-pathogen dynamics are influenced by two infection-induced behavioral changes. RABV-infected hosts often exhibit increased aggression which facilitates transmission, and rabies also leads to reduced activity and paralysis prior to death. Although several studies document rabies-induced behavioral changes in rodents and other dead-end hosts, surprisingly few studies have measured these changes in vampire bats, the key natural reservoir throughout Latin America. Here, we take advantage of an experiment designed to test the safety and efficacy of an oral rabies vaccine in captive male vampire bats to quantify for the first time how rabies affects allogrooming and aggressive behaviors in the vampire bat. Compared to non-rabid vampire bats, rabid individuals reduced their allogrooming prior to death, but we did not detect increases in aggression among bats. To put our results in context, we review what is known and what remains unclear about behavioral changes of rabid vampire bats.

Biology Letters↗

USGS2021

Causes of delayed outbreak responses and their impacts on epidemic spread

Livestock diseases have devastating consequences economically, socially and politically across the globe. In certain systems, pathogens remain viable after host death, which enables residual transmissions from infected carcasses. Rapid culling and carcass disposal are well-established strategies for stamping out an outbreak and limiting its impact; however, wait-times for these procedures, i.e. response delays, are typically farm-specific and time-varying due to logistical constraints. Failing to incorporate variable response delays in epidemiological models may understate outbreak projections and mislead management decisions. We revisited the 2001 foot-and-mouth epidemic in the United Kingdom and sought to understand how misrepresented response delays can influence model predictions. Survival analysis identified farm size and control demand as key factors that impeded timely culling and disposal activities on individual farms. Using these factors in the context of an existing policy to predict local variation in response times significantly affected predictions at the national scale. Models that assumed fixed, timely responses grossly underestimated epidemic severity and its long-term consequences. As a result, this study demonstrates how general inclusion of response dynamics and recognition of partial controllability of interventions can help inform management priorities during epidemics of livestock diseases.

Journal of the Royal Society Interface↗

USGS2024

Chytrid infections exhibit historical spread and contemporary seasonality in a declining stream-breeding frog

Species with extensive geographical ranges pose special challenges to assessing drivers of wildlife disease, necessitating collaborative and large-scale analyses. The imperilled foothill yellow-legged frog ( Rana boylii ) inhabits a wide geographical range and variable conditions in rivers of California and Oregon (USA), and is considered threatened by the pathogen Batrachochytrium dendrobatidis (Bd). To assess drivers of Bd infections over time and space, we compiled over 2000 datapoints from R. boylii museum specimens (collected 1897–2005) and field samples (2005–2021) spanning 9° of latitude. We observed a south-to-north spread of Bd detections beginning in the 1940s and increase in prevalence from the 1940s to 1970s, coinciding with extirpation from southern latitudes. We detected eight high-prevalence geographical clusters through time that span the species' geographical range. Field-sampled male R. boylii exhibited the highest prevalence, and juveniles sampled in autumn exhibited the highest loads. Bd infection risk was highest in lower elevation rain-dominated watersheds, and with cool temperatures and low stream-flow conditions at the end of the dry season. Through a holistic assessment of relationships between infection risk, geographical context and time, we identify the locations and time periods where Bd mitigation and monitoring will be critical for conservation of this imperilled species.

California↗

USGS2026

Small cumulative survival costs of enzootic disease could suppress long-term population size

Fungal pathogens can cause epizootics that result in widespread mortality and rapid population declines in some species. However, even in the absence of high disease-induced mortality, enzootic mycoses could have large-scale impacts on host population dynamics. Here, we examined the effects of ophidiomycosis, an enzootic fungal disease, on a Louisiana snake community over a 3-year period using a multi-state Jolly–Seber model with disease-state misclassification. We did not detect a difference between the average weekly apparent survival probability of uninfected and infected hosts for either Nerodia species or Thamnophis proximus . We also found a strong positive association between snout-to-vent length and weekly apparent survival probability across all species. We found that recruitment of infected hosts was slightly higher than recruitment of uninfected hosts for two of the three species. Population projections suggested divergent trajectories between disease-present and disease-absent scenarios, where disease-absent populations had higher abundance than disease-present populations. Our results highlight that small differences in survival can accumulate over time, as well as the challenges of quantifying population-level impacts of enzootic diseases when survival differences are not readily detected, underscoring the importance of continued long-term monitoring to assess whether ophidiomycosis affects snake population dynamics.

Louisiana↗

USGS2008

Extreme endurance flights by landbirds crossing the Pacific Ocean: Ecological corridor rather than barrier?

Mountain ranges, deserts, ice fields and oceans generally act as barriers to the movement of land-dependent animals, often profoundly shaping migration routes. We used satellite telemetry to track the southward flights of bar-tailed godwits (Limosa lapponica baueri), shorebirds whose breeding and non-breeding areas are separated by the vast central Pacific Ocean. Seven females with surgically implanted transmitters flew non-stop 8117-11680km (10153??1043 s.d.) directly across the Pacific Ocean; two males with external transmitters flew non-stop along the same corridor for 7008-7390km. Flight duration ranged from 6.0 to 9.4 days (7.8??1.3 s.d.) for birds with implants and 5.0 to 6.6 days for birds with externally attached transmitters. These extraordinary non-stop flights establish new extremes for avian flight performance, have profound implications for understanding the physiological capabilities of vertebrates and how birds navigate, and challenge current physiological paradigms on topics such as sleep, dehydration and phenotypic flexibility. Predicted changes in climatic systems may affect survival rates if weather conditions at their departure hub or along the migration corridor should change. We propose that this transoceanic route may function as an ecological corridor rather than a barrier, providing a wind-assisted passage relatively free of pathogens and predators. ?? 2008 The Royal Society.

Proceedings of the Royal Society B: Biological Sci↗

USGS2009

Does influenza A affect body condition of wild mallard ducks, or vice versa?

Low pathogenic avian influenza (LPAI) viruses are well documented to circulate within wild waterfowl populations (Olsen et. al. 2006 ). It has been assumed that these infections are benign with no subsequent effects on life-history parameters. The study by Latorre-Margalef et al. (2009 ; hereafter L.-M. et al. ) represents an important step, as they attempt to test this assumption in wild birds. L.-M. et al. captured migrating mallards ( Anas platyrhynchos ) at a staging area and tested them for the presence of avian influenza A virus (IAV). They related IAV infection status to body mass and duration of time spent on the staging area. Overall, the study is well designed with impressive sample sizes and the analyses are carefully conducted and presented. However, in discussing these results, the authors assume causation based upon correlation and, although they acknowledge the possibility of immunosuppression during migration due to reduced energy stores, they do not discuss it as a possible explanation for their findings. Below, we consider several of the major findings by L.-M. et al. , providing alternative explanations for the results. Because the L.-M. et al. study design is correlational, it is not possible to use their data to distinguish between their interpretations and our alternative explanations.

Proceedings of the Royal Society B: Biological Sci↗

USGS2018

The ecology of movement and behaviour: a saturated tripartite network for describing animal contacts

Ecologists regularly use animal contact networks to describe interactions underlying pathogen transmission, gene flow, and information transfer. However, empirical descriptions of contact often overlook some features of individual movement, and decisions about what kind of network to use in a particular setting are commonly ad hoc . Here, we relate individual movement trajectories to contact networks through a tripartite network model of individual, space, and time nodes. Most networks used in animal contact studies (e.g. individual association networks, home range overlap networks, and spatial networks) are simplifications of this tripartite model. The tripartite structure can incorporate a broad suite of alternative ecological metrics like home range sizes and patch occupancy patterns into inferences about contact network metrics such as modularity and degree distribution. We demonstrate the model's utility with two simulation studies using alternative forms of ecological data to constrain the tripartite network's structure and inform expectations about the harder-to-measure metrics related to contact.

Proceedings of the Royal Society B: Biological Sci↗

USGS2022

Avian influenza antibody prevalence increases with mercury contamination in wild waterfowl

Environmental contamination is widespread and can negatively impact wildlife health. Some contaminants, including heavy metals, have immunosuppressive effects, but prior studies have rarely measured contamination and disease simultaneously, which limits our understanding of how contaminants and pathogens interact to influence wildlife health. Here, we measured mercury concentrations, influenza infection, influenza antibodies, and body condition in 749 individuals from 11 species of wild ducks overwintering in California. We found that the odds of prior influenza infection increased more than five-fold across the observed range of blood mercury concentrations, while accounting for species, age, sex, and date. The prevalence of influenza infection was also higher in species with higher average mercury concentrations. We detected no relationship between influenza infection and body fat content. This positive relationship between influenza prevalence and mercury concentrations in migratory waterfowl suggests that immunotoxic effects of mercury contamination could promote the spread of avian influenza along migratory flyways, especially if influenza has minimal effects on bird health and mobility. More generally, these results show that the effects of environmental contamination could extend beyond the geographic area of contamination itself by altering the prevalence of infectious diseases in highly mobile hosts.

Proceedings of the Royal Society B↗

USGS2024

A systematic review of laboratory investigations into the pathogenesis of avian influenza viruses in wild avifauna of North America

The lack of consolidated information regarding the response of wild bird species to infection with avian influenza virus (AIV) is a challenge to both conservation managers and researchers alike, with related sectors also impacted, such as public health and commercial poultry. Using two independent searches, we reviewed published literature for studies describing wild bird species experimentally infected with avian influenza to assess host species’ relative susceptibility to AIVs. Additionally, we summarize broad-scale parameters for elements such as shedding duration and minimum infectious dose that can be used in transmission modelling efforts. Our synthesis shows that waterfowl (i.e. Anatidae) compose the vast majority of published AIV pathobiology studies, whereas gulls and passerines are less represented in research despite evidence that they also are susceptible and contribute to highly pathogenic avian influenza disease dynamics. This study represents the first comprehensive effort to compile available literature regarding the pathobiology of AIVs in all wild birds in over a decade. This database can now serve as a tool to all researchers, providing generalized estimates of pathobiology parameters for a variety of wild avian families and an opportunity to critically examine and assess what is known and identify where further insight is needed.

Proceeding of the Royal Society B↗

USGS2017

Lyme disease ecology in a changing world: Consensus, uncertainty and critical gaps for improving control

Lyme disease is the most common tick-borne disease in temperate regions of North America, Europe and Asia, and the number of reported cases has increased in many regions as landscapes have been altered. Although there has been extensive work on the ecology and epidemiology of this disease in both Europe and North America, substantial uncertainty exists about fundamental aspects that determine spatial and temporal variation in both disease risk and human incidence, which hamper effective and efficient prevention and control. Here we describe areas of consensus that can be built on, identify areas of uncertainty and outline research needed to fill these gaps to facilitate predictive models of disease risk and the development of novel disease control strategies. Key areas of uncertainty include: (i) the precise influence of deer abundance on tick abundance, (ii) how tick populations are regulated, (iii) assembly of host communities and tick-feeding patterns across different habitats, (iv) reservoir competence of host species, and (v) pathogenicity for humans of different genotypes of Borrelia burgdorferi . Filling these knowledge gaps will improve Lyme disease prevention and control and provide general insights into the drivers and dynamics of this emblematic multi-host–vector-borne zoonotic disease.

Philosophical Transactions of the Royal Society B:↗

USGS2016

Mitigating amphibian chytridiomycosis in nature

Amphibians across the planet face the threat of population decline and extirpation caused by the disease chytridiomycosis. Despite consensus that the fungal pathogens responsible for the disease are conservation issues, strategies to mitigate their impacts in the natural world are, at best, nascent. Reducing risk associated with the movement of amphibians, non-amphibian vectors and other sources of infection remains the first line of defence and a primary objective when mitigating the threat of disease in wildlife. Amphibian-associated chytridiomycete fungi and chytridiomycosis are already widespread, though, and we therefore focus on discussing options for mitigating the threats once disease emergence has occurred in wild amphibian populations. All strategies have shortcomings that need to be overcome before implementation, including stronger efforts towards understanding and addressing ethical and legal considerations. Even if these issues can be dealt with, all currently available approaches, or those under discussion, are unlikely to yield the desired conservation outcome of disease mitigation. The decision process for establishing mitigation strategies requires integrated thinking that assesses disease mitigation options critically and embeds them within more comprehensive strategies for the conservation of amphibian populations, communities and ecosystems.

Philosophical Transactions of the Royal Society B:↗

USGS2000

Genetic analyses reveal unusually high diversity of infectious haematopoietic necrosis virus in rainbow trout aquaculture

Infectious haematopoietic necrosis virus (IHNV) is the most significant virus pathogen of salmon and trout in North America. Previous studies have shown relatively low genetic diversity of IHNV within large geographical regions. In this study, the genetic heterogeneity of 84 IHNV isolates sampled from rainbow trout ( Oncorhynchus mykiss ) over a 20 year period at four aquaculture facilities within a 12 mile stretch of the Snake River in Idaho, USA was investigated. The virus isolates were characterized using an RNase protection assay (RPA) and nucleotide sequence analyses. Among the 84 isolates analysed, 46 RPA haplotypes were found and analyses revealed a high level of genetic heterogeneity relative to that detected in other regions. Sequence analyses revealed up to 7·6% nucleotide divergence, which is the highest level of diversity reported for IHNV to date. Phylogenetic analyses identified four distinct monophyletic clades representing four virus lineages. These lineages were distributed across facilities, and individual facilities contained multiple lineages. These results suggest that co-circulating IHNV lineages of relatively high genetic diversity are present in the IHNV populations in this rainbow trout culture study site. Three of the four lineages exhibited temporal trends consistent with rapid evolution.

Journal of General Virology↗

USGS1965

Characteristics and identification of oxidative Pseudomonads isolated from diseased fish

Several characteristics of 20 strains of oxidative pseudomonads, all but one of which were isolated from freshwater fish, were determined. All strains oxidized glucose and gluconate, produced NH 3 from 1 % peptone, grew at 6, 12, 20 and 30° and produced cytochrome oxidase. Lipase was produced by 17 of the strains, while 15 produced gelatinase, and 16 produced fluorescent pigment. These and other characteristics used to identify fish-spoilage pseudomonads are also useful for identification of fish-pathogenic pseudomonads. Species determinations from the present data were not attempted. However, from previously published data on speciation of Pseudomonas , most of the 20 strains appeared to be closely related to or identical with P. fluorescens .

Journal of General Microbiology↗

USGS2024

Local and systemic replicative fitness for viruses in specialist, generalist, and non-specialist interactions with salmonid hosts

Host tissues represent diverse resources or barriers for pathogen replicative fitness. We tested whether viruses in specialist, generalist, and non-specialist interactions replicate differently in local entry tissue (fin), and systemic target tissue (kidney) using infectious hematopoietic necrosis virus (IHNV) and three salmonid fish hosts. Virus tissue replication was host specific, but one feature was shared by specialists and the generalist which was uncommon in the non-specialist interactions: high host entry and replication capacity in the local tissue after contact. Moreover, specialists showed increased replication in systemic target tissues early after host contact. By comparing ancestral and derived IHNV viruses, we also characterized replication tradeoffs associated with specialist and generalist evolution. Compared with the ancestral virus, a derived specialist gained early local replicative fitness in the new host but lost replicative fitness in the ancestral host. By contrast, a derived generalist showed small replication losses relative to the ancestral virus in the ancestral host but increased early replication in the local tissue of novel hosts. This study shows that the mechanisms of specialism and generalism are host specific and that local and systemic replication can contribute differently to overall within host replicative fitness for specialist and generalist viruses.

Journal of General Virology↗

USGS2024

Metagenomic sequencing sheds light on microbes putatively associated with pneumonia-related fatalities of white-tailed deer (Odocoileus virginianus)

With emerging infectious disease outbreaks in human, domestic and wild animal populations on the rise, improvements in pathogen characterization and surveillance are paramount for the protection of human and animal health, as well as the conservation of ecologically and economically important wildlife. Genomics offers a range of suitable tools to meet these goals, with metagenomic sequencing facilitating the characterization of whole microbial communities associated with emerging and endemic disease outbreaks. Here, we use metagenomic sequencing in a case-control study to identify microbes in lung tissue associated with newly observed pneumonia-related fatalities in 34 white-tailed deer ( Odocoileus virginianus ) in Wisconsin, USA. We identified 20 bacterial species that occurred in more than a single individual. Of these, only Clostridium novyi was found to substantially differ (in number of detections) between case and control sample groups; however, this difference was not statistically significant. We also detected several bacterial species associated with pneumonia and/or other diseases in ruminants ( Mycoplasma ovipneumoniae , Trueperella pyogenes , Pasteurella multocida , Anaplasma phagocytophilum , Fusobacterium necrophorum ); however, these species did not substantially differ between case and control sample groups. On average, we detected a larger number of bacterial species in case samples than controls, supporting the potential role of polymicrobial infections in this system. Importantly, we did not detect DNA of viruses or fungi, suggesting that they are not significantly associated with pneumonia in this system. Together, these results highlight the utility of metagenomic sequencing for identifying disease-associated microbes. This preliminary list of microbes will help inform future research on pneumonia-associated fatalities of white-tailed deer.

Microbial Genomics↗

USGS2003

Phylogeography of infectious haematopoietic necrosis virus in North America

Infectious hematopoietic necrosis virus (IHNV) is a rhabdoviral pathogen that infects wild and cultured salmonid fish throughout the Pacific Northwest of North America. IHNV causes severe epidemics in young fish and can cause disease or occur asymptomatically in adults. In a broad survey of 323 IHNV field isolates, sequence analysis of a 303 nucleotide variable region within the glycoprotein gene revealed a maximum nucleotide diversity of 8·6 %, indicating low genetic diversity overall for this virus. Phylogenetic analysis revealed three major virus genogroups, designated U, M and L, which varied in topography and geographical range. Intragenogroup genetic diversity measures indicated that the M genogroup had three- to fourfold more diversity than the other genogroups and suggested relatively rapid evolution of the M genogroup and stasis within the U genogroup. We speculate that factors influencing IHNV evolution may have included ocean migration ranges of their salmonid host populations and anthropogenic effects associated with fish culture.

Journal of General Virology↗

USGS2013

Spatio-temporal dynamics of pneumonia in bighorn sheep

Bighorn sheep mortality related to pneumonia is a primary factor limiting population recovery across western North America, but management has been constrained by an incomplete understanding of the disease. We analysed patterns of pneumonia-caused mortality over 14 years in 16 interconnected bighorn sheep populations to gain insights into underlying disease processes. 2. We observed four age-structured classes of annual pneumonia mortality patterns: all-age, lamb-only, secondary all-age and adult-only. Although there was considerable variability within classes, overall they differed in persistence within and impact on populations. Years with pneumonia-induced mortality occurring simultaneously across age classes (i.e. all-age) appeared to be a consequence of pathogen invasion into a naïve population and resulted in immediate population declines. Subsequently, low recruitment due to frequent high mortality outbreaks in lambs, probably due to association with chronically infected ewes, posed a significant obstacle to population recovery. Secondary all-age events occurred in previously exposed populations when outbreaks in lambs were followed by lower rates of pneumonia-induced mortality in adults. Infrequent pneumonia events restricted to adults were usually of short duration with low mortality. 3. Acute pneumonia-induced mortality in adults was concentrated in fall and early winter around the breeding season when rams are more mobile and the sexes commingle. In contrast, mortality restricted to lambs peaked in summer when ewes and lambs were concentrated in nursery groups. 4. We detected weak synchrony in adult pneumonia between adjacent populations, but found no evidence for landscape-scale extrinsic variables as drivers of disease. 5. We demonstrate that there was a >60% probability of a disease event each year following pneumonia invasion into bighorn sheep populations. Healthy years also occurred periodically, and understanding the factors driving these apparent fade-out events may be the key to managing this disease. Our data and modelling indicate that pneumonia can have greater impacts on bighorn sheep populations than previously reported, and we present hypotheses about processes involved for testing in future investigations and management.

Journal of Animal Ecology↗