RESUMO
Environmental pathogen reservoirs exist for many globally important diseases and can fuel epidemics, influence pathogen evolution, and increase the threat of host extinction. Species composition can be an important factor that shapes reservoir dynamics and ultimately determines the outcome of a disease outbreak. However, disease-induced mortality can change species communities, indicating that species responsible for environmental reservoir maintenance may change over time. Here we examine the reservoir dynamics of Pseudogymnoascus destructans, the fungal pathogen that causes white-nose syndrome in bats. We quantified changes in pathogen shedding, infection prevalence and intensity, host abundance, and the subsequent propagule pressure imposed by each species over time. We find that highly shedding species are important during pathogen invasion, but contribute less over time to environmental contamination as they also suffer the greatest declines. Less infected species remain more abundant, resulting in equivalent or higher propagule pressure. More broadly, we demonstrate that high infection intensity and subsequent mortality during disease progression can reduce the contributions of high-shedding species to long-term pathogen maintenance.
RESUMO
Demographic factors are fundamental in shaping infectious disease dynamics. Aspects of populations that create structure, like age and sex, can affect patterns of transmission, infection intensity and population outcomes. However, studies rarely link these processes from individual to population-scale effects. Moreover, the mechanisms underlying demographic differences in disease are frequently unclear. Here, we explore sex-biased infections for a multi-host fungal disease of bats, white-nose syndrome, and link disease-associated mortality between sexes, the distortion of sex ratios and the potential mechanisms underlying sex differences in infection. We collected data on host traits, infection intensity and survival of five bat species at 42 sites across seven years. We found females were more infected than males for all five species. Females also had lower apparent survival over winter and accounted for a smaller proportion of populations over time. Notably, female-biased infections were evident by early hibernation and likely driven by sex-based differences in autumn mating behaviour. Male bats were more active during autumn which likely reduced replication of the cool-growing fungus. Higher disease impacts in female bats may have cascading effects on bat populations beyond the hibernation season by limiting recruitment and increasing the risk of Allee effects.
Assuntos
Quirópteros , Hibernação , Micoses , Feminino , Masculino , Animais , Animais Selvagens , Quirópteros/microbiologia , Micoses/epidemiologia , Micoses/veterinária , Micoses/microbiologia , FungosRESUMO
Understanding host persistence with emerging pathogens is essential for conserving populations. Hosts may initially survive pathogen invasions through pre-adaptive mechanisms. However, whether pre-adaptive traits are directionally selected to increase in frequency depends on the heritability and environmental dependence of the trait and the costs of trait maintenance. Body condition is likely an important pre-adaptive mechanism aiding in host survival, although can be seasonally variable in wildlife hosts. We used data collected over 7 years on bat body mass, infection and survival to determine the role of host body condition during the invasion and establishment of the emerging disease, white-nose syndrome. We found that when the pathogen first invaded, bats with higher body mass were more likely to survive, but this effect dissipated following the initial epizootic. We also found that heavier bats lost more weight overwinter, but fat loss depended on infection severity. Lastly, we found mixed support that bat mass increased in the population after pathogen arrival; high annual plasticity in individual bat masses may have reduced the potential for directional selection. Overall, our results suggest that some factors that contribute to host survival during pathogen invasion may diminish over time and are potentially replaced by other host adaptations.
Assuntos
Quirópteros , Animais , Animais Selvagens , FenótipoRESUMO
Emerging infectious diseases can have devastating effects on host communities, causing population collapse and species extinctions. The timing of novel pathogen arrival into naïve species communities can have consequential effects that shape the trajectory of epidemics through populations. Pathogen introductions are often presumed to occur when hosts are highly mobile. However, spread patterns can be influenced by a multitude of other factors including host body condition and infectiousness. White-nose syndrome (WNS) is a seasonal emerging infectious disease of bats, which is caused by the fungal pathogen Pseudogymnoascus destructans. Within-site transmission of P. destructans primarily occurs over winter; however, the influence of bat mobility and infectiousness on the seasonal timing of pathogen spread to new populations is unknown. We combined data on host population dynamics and pathogen transmission from 22 bat communities to investigate the timing of pathogen arrival and the consequences of varying pathogen arrival times on disease impacts. We found that midwinter arrival of the fungus predominated spread patterns, suggesting that bats were most likely to spread P. destructans when they are highly infectious, but have reduced mobility. In communities where P. destructans was detected in early winter, one species suffered higher fungal burdens and experienced more severe declines than at sites where the pathogen was detected later in the winter, suggesting that the timing of pathogen introduction had consequential effects for some bat communities. We also found evidence of source-sink population dynamics over winter, suggesting some movement among sites occurs during hibernation, even though bats at northern latitudes were thought to be fairly immobile during this period. Winter emergence behaviour symptomatic of white-nose syndrome may further exacerbate these winter bat movements to uninfected areas. Our results suggest that low infectiousness during host migration may have reduced the rate of expansion of this deadly pathogen, and that elevated infectiousness during winter plays a key role in seasonal transmission. Furthermore, our results highlight the importance of both accurate estimation of the timing of pathogen spread and the consequences of varying arrival times to prevent and mitigate the effects of infectious diseases.
Assuntos
Ascomicetos , Quirópteros , Hibernação , Animais , NarizRESUMO
Habitat alteration can influence suitability, creating ecological traps where habitat preference and fitness are mismatched. Despite their importance, ecological traps are notoriously difficult to identify and their impact on host-pathogen dynamics remains largely unexplored. Here we assess individual bat survival and habitat preferences in the midwestern United States before, during, and after the invasion of the fungal pathogen that causes white-nose syndrome. Despite strong selection pressures, most hosts continued to select habitats where disease severity was highest and survival was lowest, causing continued population declines. However, some individuals used refugia where survival was higher. Over time, a higher proportion of the total population used refugia than before pathogen arrival. Our results demonstrate that host preferences for habitats with high disease-induced mortality can create ecological traps that threaten populations, even in the presence of accessible refugia.
Assuntos
Doenças dos Animais , Quirópteros , Ecossistema , Sobrevida , Doenças dos Animais/microbiologia , Doenças dos Animais/mortalidade , Animais , Ascomicetos , Quirópteros/microbiologia , Conservação dos Recursos Naturais , Fungos/patogenicidade , Michigan , Nariz , Dinâmica Populacional , Temperatura , WisconsinRESUMO
Disease outbreaks and pathogen introductions can have significant effects on host populations, and the ability of pathogens to persist in the environment can exacerbate disease impacts by fueling sustained transmission, seasonal epidemics, and repeated spillover events. While theory suggests that the presence of an environmental reservoir increases the risk of host declines and threat of extinction, the influence of reservoir dynamics on transmission and population impacts remains poorly described. Here we show that the extent of the environmental reservoir explains broad patterns of host infection and the severity of disease impacts of a virulent pathogen. We examined reservoir and host infection dynamics and the resulting impacts of Pseudogymnoascus destructans, the fungal pathogen that causes white-nose syndrome, in 39 species of bats at 101 sites across the globe. Lower levels of pathogen in the environment consistently corresponded to delayed infection of hosts, fewer and less severe infections, and reduced population impacts. In contrast, an extensive and persistent environmental reservoir led to early and widespread infections and severe population declines. These results suggest that continental differences in the persistence or decay of P. destructans in the environment altered infection patterns in bats and influenced whether host populations were stable or experienced severe declines from this disease. Quantifying the impact of the environmental reservoir on disease dynamics can provide specific targets for reducing pathogen levels in the environment to prevent or control future epidemics.
Assuntos
Quirópteros/microbiologia , Reservatórios de Doenças/microbiologia , Micoses/epidemiologia , Animais , Ascomicetos/patogenicidade , Epidemias , Hibernação , Micoses/microbiologia , Nariz/microbiologia , Doenças Nasais/epidemiologia , Doenças Nasais/microbiologia , Dinâmica Populacional , Estações do AnoRESUMO
Tools for reducing wildlife disease impacts are needed to conserve biodiversity. White-nose syndrome (WNS), caused by the fungus Pseudogymnoascus destructans, has caused widespread declines in North American bat populations and threatens several species with extinction. Few tools exist for managers to reduce WNS impacts. We tested the efficacy of a probiotic bacterium, Pseudomonas fluorescens, to reduce impacts of WNS in two simultaneous experiments with caged and free-flying Myotis lucifugus bats at a mine in Wisconsin, USA. In the cage experiment there was no difference in survival between control and P. fluorescens-treated bats. However, body mass, not infection intensity, predicted mortality, suggesting that within-cage disturbance influenced the cage experiment. In the free-flying experiment, where bats were able to avoid conspecific disturbance, infection intensity predicted the date of emergence from the mine. In this experiment treatment with P. fluorescens increased apparent overwinter survival five-fold compared to the control group (from 8.4% to 46.2%) by delaying emergence of bats from the site by approximately 32 days. These results suggest that treatment of bats with P. fluorescens may substantially reduce WNS mortality, and, if used in combination with other interventions, could stop population declines.
Assuntos
Ascomicetos/fisiologia , Fenômenos Fisiológicos Bacterianos , Quirópteros/microbiologia , Probióticos/farmacologia , AnimaisRESUMO
In Fig. 3d this Letter, the R2 value should have been '0.19' instead of '0.66'; this has been corrected online.
RESUMO
White-nose syndrome (WNS) affects bats primarily in winter, with Pseudogymnoascus destructans, the fungus that causes WNS, growing on bats in colder climates as they are hibernating. As a result, nearly all disease investigations have been conducted on bats in the winter or as they are emerging in spring. Although P. destructans has been detected on bats during the summer season, the seasonal dynamics of infection during this period remain poorly understood. To test for the presence of P. destructans during the summer season, we sampled bats that were free flying from June 2017 to September 2017 and also sampled bats from a maternity roost in August and outside a known hibernaculum in September. We collected skin swabs from the muzzle and forearm of bats, and using real-time PCR methods, we detected P. destructans DNA on 16% (12/76) of bats sampled in Wisconsin, US, including juvenile little brown bats (Myotis lucifugus) from bat house maternity roosts, and free-flying adult bats of two species captured in June, the little brown bat and the migratory eastern red bat (Lasiurus borealis). These data illustrated the potential for P. destructans to be transferred and dispersed among bats during the summer and highlighted the complex seasonal dynamics associated with this pathogen.
Assuntos
Ascomicetos/isolamento & purificação , Quirópteros/microbiologia , Dermatomicoses/veterinária , Estações do Ano , Animais , Dermatomicoses/epidemiologia , Dermatomicoses/microbiologia , Feminino , Masculino , Wisconsin/epidemiologiaRESUMO
Understanding host interactions that lead to pathogen transmission is fundamental to the prediction and control of epidemics1-5. Although the majority of transmissions often occurs within social groups6-9, the contribution of connections that bridge groups and species to pathogen dynamics is poorly understood10-12. These cryptic connections-which are often indirect or infrequent-provide transmission routes between otherwise disconnected individuals and may have a key role in large-scale outbreaks that span multiple populations or species. Here we quantify the importance of cryptic connections in disease dynamics by simultaneously characterizing social networks and tracing transmission dynamics of surrogate-pathogen epidemics through eight communities of bats. We then compared these data to the invasion of the fungal pathogen that causes white-nose syndrome, a recently emerged disease that is devastating North American bat populations13-15. We found that cryptic connections increased links between individuals and between species by an order of magnitude. Individuals were connected, on average, to less than two per cent of the population through direct contact and to only six per cent through shared groups. However, tracing surrogate-pathogen dynamics showed that each individual was connected to nearly fifteen per cent of the population, and revealed widespread transmission between solitarily roosting individuals as well as extensive contacts among species. Connections estimated from surrogate-pathogen epidemics, which include cryptic connections, explained three times as much variation in the transmission of the fungus that causes white-nose syndrome as did connections based on shared groups. These findings show how cryptic connections facilitate the community-wide spread of pathogens and can lead to explosive epidemics.
Assuntos
Ascomicetos/patogenicidade , Quirópteros/microbiologia , Busca de Comunicante/veterinária , Transmissão de Doença Infecciosa/veterinária , Micoses/veterinária , Sistemas de Identificação Animal , Animais , Controle de Doenças Transmissíveis , Busca de Comunicante/métodos , Transmissão de Doença Infecciosa/estatística & dados numéricos , Poeira/análise , Hibernação , Humanos , Masculino , Micoses/epidemiologia , Micoses/microbiologia , Micoses/transmissão , Rede Social , Zoonoses/microbiologia , Zoonoses/transmissãoRESUMO
Before the discovery of white-nose syndrome (WNS), a fungal disease caused by Pseudogymnoascus destructans, there were no reports of fungal skin infections in bats during hibernation. In 2011, bats with grossly visible fungal skin infections similar in appearance to WNS were reported from multiple sites in Wisconsin, US, a state outside the known range of P. destructans and WNS at that time. Tape impressions or swab samples were collected from affected areas of skin from bats with these fungal infections in 2012 and analyzed by microscopy, culture, or direct DNA amplification and sequencing of the fungal internal transcribed spacer region (ITS). A psychrophilic species of Trichophyton was isolated in culture, detected by direct DNA amplification and sequencing, and observed on tape impressions. Deoxyribonucleic acid indicative of the same fungus was also detected on three of five bat carcasses collected in 2011 and 2012 from Wisconsin, Indiana, and Texas, US. Superficial fungal skin infections caused by Trichophyton sp. were observed in histopathology for all three bats. Sequencing of the ITS of Trichophyton sp., along with its inability to grow at 25 C, indicated that it represented a previously unknown species, described herein as Trichophyton redellii sp. nov. Genetic diversity present within T. redellii suggests it is native to North America but that it had been overlooked before enhanced efforts to study fungi associated with bats in response to the emergence of WNS.