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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:↗

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:↗

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↗

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↗

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↗

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↗

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↗

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↗

Contact and contagion: Probability of transmission given contact varies with demographic state in bighorn sheep

Understanding both contact and probability of transmission given contact are key to managing wildlife disease. However, wildlife disease research tends to focus on contact heterogeneity, in part because the probability of transmission given contact is notoriously difficult to measure. Here, we present a first step towards empirically investigating the probability of transmission given contact in free-ranging wildlife. We used measured contact networks to test whether bighorn sheep demographic states vary systematically in infectiousness or susceptibility to Mycoplasma ovipneumoniae , an agent responsible for bighorn sheep pneumonia. We built covariates using contact network metrics, demographic information and infection status, and used logistic regression to relate those covariates to lamb survival. The covariate set contained degree, a classic network metric describing node centrality, but also included covariates breaking the network metrics into subsets that differentiated between contacts with yearlings, ewes with lambs, and ewes without lambs, and animals with and without active infections. Yearlings, ewes with lambs, and ewes without lambs showed similar group membership patterns, but direct interactions involving touch occurred at a rate two orders of magnitude higher between lambs and reproductive ewes than between any classes of adults or yearlings, and one order of magnitude higher than direct interactions between multiple lambs. Although yearlings and non-reproductive bighorn ewes regularly carried M. ovipneumoniae , our models suggest that a contact with an infected reproductive ewe had approximately five times the odds of producing a lamb mortality event of an identical contact with an infected dry ewe or yearling. Consequently, management actions targeting infected animals might lead to unnecessary removal of young animals that carry pathogens but rarely transmit. This analysis demonstrates a simple logistic regression approach for testing a priori hypotheses about variation in the odds of transmission given contact for free-ranging hosts, and may be broadly applicable for investigations in wildlife disease ecology.

Journal of Animal Ecology↗

Context-dependent variation in persistence of host populations in the face of disease

Research Highlight : Valenzuela-Sánchez, A., Azat, C., Cunningham, A. A., Delgado, S., Bacigalupe, L. D., Beltrand, J., Serrano, J. M., Sentenac, H., Haddow, N., Toledo, V., Schmidt, B. R., & Cayuela, H. (2022). Interpopulation differences in male reproductive effort drive the population dynamics of a host exposed to an emerging fungal pathogen. Journal of Animal Ecology , 00 , 1– 12. https://doi.org/10.1111/1365-2656.13603 . Understanding the nuances of population persistence in the face of a stressor can help predict extinction risk and guide conservation actions. However, the exact mechanisms driving population stability may not always be known. In this paper, Valenzuela-Sánchez et al. (2022) integrate long-term mark–recapture data, focal measurements of reproductive effort, a population matrix model and inferences on life-history variation to reveal differences in demographic response to disease in a susceptible frog species ( Rhinoderma darwinii ). Valenzuela-Sánchez et al. found that demographic compensation via recruitment explained the positive population growth rate in their high disease prevalence population whereas the low disease prevalence population did not compensate and thus had decreasing population growth. Compensatory recruitment was likely due to the high probability of males brooding, and the high number of brooded larvae in the high prevalence population compared to low prevalence and disease-free populations. Valenzuela-Sánchez et al. also document faster generation times in the high prevalence population, which may indicate a faster life history that may be contributing to the population's ability to compensate for reduced survival. Lastly, the authors find a positive relationship between disease prevalence and the proportion of juveniles in a given population that suggest that there may be a threshold for disease prevalence that triggers increased reproductive effort. Altogether, their study provides novel support for increased reproductive effort as the pathway for compensatory recruitment leading to increasing population growth despite strong negative effects of disease on adult survival. Their results also caution the overgeneralization of the effects of stressors (e.g. disease) on population dynamics, where context-dependent responses may differ among host populations of a given species.

Journal of Animal Ecology↗

Examination of the interaction between age-specific predation and chronic disease in the Greater Yellowstone Ecosystem

Predators may create healthier prey populations by selectively removing diseased individuals. Predators typically prefer some ages of prey over others, which may, or may not, align with those prey ages that are most likely to be diseased. The interaction of age-specific infection and predation has not been previously explored and likely has sizable effects on disease dynamics. We hypothesize that predator cleansing effects will be greater when the disease and predation occur in the same prey age groups. We examine the predator cleansing effect using a model where both vulnerability to predators and pathogen prevalence vary with age. We tailor this model to chronic wasting disease (CWD) in mule deer and elk populations in the Greater Yellowstone Ecosystem, with empirical data from Yellowstone grey wolves and cougars. Model results suggest that under moderate, yet realistic, predation pressure from cougars and wolves independently, predators may decrease CWD outbreak size substantially and delay the accumulation of symptomatic deer and elk. The magnitude of this effect is driven by the ability of predators to selectively remove late-stage CWD infections that are likely the most responsible for transmission, but this may not be the age class they typically select. Thus, predators that select for infected young adults over uninfected juveniles have a stronger cleansing effect, and these effects are strengthened when transmission rates increase with increasing prey morbidity. There are also trade-offs from a management perspective—that is, increasing predator kill rates can result in opposing forces on prey abundance and CWD prevalence. Our modelling exploration shows that predators have the potential to reduce prevalence in prey populations when prey age and disease severity are considered, yet the strength of this effect is influenced by predators' selection for demography or body condition. Current CWD management focuses on increasing cervid hunting as the primary management tool, and our results suggest predators may also be a useful tool under certain conditions, but not necessarily without additional impacts on host abundance and demography. Protected areas with predator populations will play a large role in informing the debate over predator impacts on disease.

Wyoming↗

Adaptive monitoring in action: Reconsidering design-based estimators reveals underestimation of whitebark pine disease prevalence in the Greater Yellowstone Ecosystem

Identifying and understanding status and trends in ecological indicators motivates continual monitoring over decades. Many programs rely on probability surveys and their companion design-based estimators for status assessments (e.g. Horvitz–Thompson). Design-based estimators do not easily extend to trend estimation nor situations with observation errors. Field-based monitoring efforts inevitably have turnover of field crew members which may affect consistency and accuracy of data collection over time. Additionally, design-based estimators ignore the complexities of spatial and temporal heterogeneity in an ecological indicator and how this variability may be linked to environmental or biological dynamics. We propose monitoring programs should re-evaluate their prescribed statistical methods, consider model-based approaches and adapt their sampling designs as needed to improve inferences. The Greater Yellowstone Ecosystem, home to two of the most iconic U.S. National Parks, has experienced significant declines in whitebark pine Pinus albicaulis communities due to forest pathogens, insect outbreaks, wildland fires and drought. Whitebark pine is a keystone species found in mountainous environments throughout the Western U.S. and Canada. We assessed the design-based ratio estimator originally recommended for estimating prevalence of white pine blister rust Cronartium ribicola . We compared the design-based estimator to a model-based approach that accounts for the sampling design, imperfect detection and allows for infection probabilities to vary over space and time. Ignoring observation errors led to lower estimated prevalence of white pine blister rust in the general population. Using model-based approaches, we found that the probability of infection has increased since 2004. However, overall prevalence likely has not changed because of the mountain pine beetle Dendroctonus ponderosae -induced shift towards smaller diameter trees that have a lower probability of infection compared to their larger cohorts. Synthesis and Applications . Using a design-based approach to detect change in ecological indicators falls short because of the inability to account for observation errors or to explore environmental or biological factors explaining temporal dynamics. Inherently understanding the mechanisms leading to changes in an ecological indicator over time informs potential management actions. Our assessment underscores the need for continued evaluation and updating of a monitoring program's sampling design and analytical procedures to maintain relevancy.

Wyoming↗

Long‐term surveys support declines in early‐season forest plants used by bumblebees

Populations of bumble bees and other pollinators have declined over the past several decades due to numerous threats, including habitat loss and degradation. However, we can rarely investigate the role of resource loss due to a lack of detailed long‐term records of forage plants and habitats. We use 22‐year repeated surveys of more than 262 sites located in grassland, forest, and wetland habitats across Illinois, USA to explore how the abundance and richness of bumble bee food plants have changed over the period of decline of the endangered rusty patched bumble bee ( Bombus affinis ). We document a decline in abundance of bumble bee forage plants in forest understories, which our phenology analysis suggests provide the primary nectar and pollen sources for foundress queens in spring, a critical life stage in bumble bee demography. By contrast, the per‐unit area abundance of food plants in primarily midsummer‐flowering grassland and wetland habitats has not declined. However, the total area of grasslands has declined across the region resulting in a net loss of grassland resources. Synthesis and applications . Our results suggest a decline in spring‐flowering forest understory plants is a previously unappreciated bumble bee stressor, compounding factors like agricultural intensification, novel pathogen exposure, and grassland habitat loss. These findings emphasize the need for greater consideration of habitat complementarity in bumble bee conservation. We conclude that continued loss of early‐season floral resources may add additional stress to critical life stages of bumble bees and limit restoration efforts if not explicitly considered in pollinator conservation.

Illinois↗

The spatial-temporal relationship of blue-winged teal to domestic poultry: Movement state modeling of a highly mobile avian influenza host

1. Migratory waterfowl facilitate long distance dispersal of zoonotic pathogens and are increasingly recognized as contributing to the geographic spread of avian influenza viruses (AIV). AIV are globally distributed and have the potential to produce highly contagious poultry disease, economically impact both large-scale and backyard poultry producers, and raise the specter of epidemics and pandemics in human populations. 2. Because migratory waterfowl behavior varies across multiple spatial and temporal scales, the timing and distribution of wild bird AIV introductions to poultry are also heterogeneous in time and space. To help reduce economic impacts to the poultry industry and enable poultry producers to better anticipate when and where poultry outbreaks may occur, it is critically important to consider the movement ecology of the waterfowl species transporting and transmitting AIV. 3. We used telemetry for a geographically widespread and common AIV host, blue-winged teal ( Spatula discors ; BWTE), to model reservoir host movement states with respect to backyard and commercial poultry facilities in the United States. Our modeling framework enabled us to estimate wild bird proximity to poultry facilities while concurrently assessing the influence of poultry facilities on BWTE movement state transition. Our primary objective was to estimate the likelihood of duck and poultry overlap by estimating when and where BWTE were geographically closest to poultry. 4. Synthesis and applications . Migratory waterfowl facilitate dispersal of the avian influenza viruses that cause highly contagious poultry disease. Movement analysis of blue-winged teal indicates that spatio-temporal overlap between wild birds and poultry facilities varies by season, the poultry type produced (e.g., turkey, chicken), and if the facility is a commercial or backyard operation. These findings are broadly applicable to disease ecology research and can be applied by poultry producers to improve bio-security, enhance poultry management, and prioritize disease surveillance efforts.

Journal of Applied Ecology↗

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

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

Alaska↗

eDNAoccupancy: An R package for multi-scale occupancy modeling of environmental DNA data

In this article we describe eDNAoccupancy, an R package for fitting Bayesian, multi-scale occupancy models. These models are appropriate for occupancy surveys that include three, nested levels of sampling: primary sample units within a study area, secondary sample units collected from each primary unit, and replicates of each secondary sample unit. This design is commonly used in occupancy surveys of environmental DNA (eDNA). eDNAoccupancy allows users to specify and fit multi-scale occupancy models with or without covariates, to estimate posterior summaries of occurrence and detection probabilities, and to compare different models using Bayesian model-selection criteria. We illustrate these features by analyzing two published data sets: eDNA surveys of a fungal pathogen of amphibians and eDNA surveys of an endangered fish species.

Molecular Ecology Resources↗

Advances and applications of occupancy models

Summary: The past decade has seen an explosion in the development and application of models aimed at estimating species occurrence and occupancy dynamics while accounting for possible non-detection or species misidentification. We discuss some recent occupancy estimation methods and the biological systems that motivated their development. Collectively, these models offer tremendous flexibility, but simultaneously place added demands on the investigator. Unlike many mark–recapture scenarios, investigators utilizing occupancy models have the ability, and responsibility, to define their sample units (i.e. sites), replicate sampling occasions, time period over which species occurrence is assumed to be static and even the criteria that constitute ‘detection’ of a target species. Subsequent biological inference and interpretation of model parameters depend on these definitions and the ability to meet model assumptions. We demonstrate the relevance of these definitions by highlighting applications from a single biological system (an amphibian–pathogen system) and discuss situations where the use of occupancy models has been criticized. Finally, we use these applications to suggest future research and model development.

Methods in Ecology and Evolution↗

Long-term video surveillance and automated analyses reveal arousal patterns in groups of hibernating bats

Understanding natural behaviours is essential to determining how animals deal with new threats (e.g. emerging diseases). However, natural behaviours of animals with cryptic lifestyles, like hibernating bats, are often poorly characterized. White-nose syndrome (WNS) is an unprecedented disease threatening multiple species of hibernating bats, and pathogen-induced changes to host behaviour may contribute to mortality. To better understand the behaviours of hibernating bats and how they might relate to WNS, we developed new ways of studying hibernation across entire seasons. We used thermal-imaging video surveillance cameras to observe little brown bats ( Myotis lucifugus ) and Indiana bats ( M. sodalis ) in two caves over multiple winters. We developed new, sharable software to test for autocorrelation and periodicity of arousal signals in recorded video. We processed 740 days (17,760 hr) of video at a rate of >1,000 hr of video imagery in less than 1 hr using a desktop computer with sufficient resolution to detect increases in arousals during midwinter in both species and clear signals of daily arousal periodicity in infected M. sodalis . Our unexpected finding of periodic synchronous group arousals in hibernating bats demonstrate the potential for video methods and suggest some bats may have innate behavioural strategies for coping with WNS. Surveillance video and accessible analysis software make it now practical to investigate long-term behaviours of hibernating bats and other hard-to-study animals.

Methods in Ecology and Evolution↗