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Abstract The use of quantitative real-time PCR (qPCR) to monitor pathogens is common; however, quantitative frameworks that consider the observation process, dynamics in pathogen presence, and pathogen load are lacking. This can be problematic in the early stages of disease progression, where low level detections may be treated as ‘inconclusive’ and excluded from analyses. Alternatively, a framework that accounts for imperfect detection would provide more robust inferences. To better estimate pathogen dynamics, we developed a hierarchical multi-scale dynamic occupancy hurdle model (MS-DOHM). The model used data gathered during sampling forPseudogymnoascus destructans (Pd), the causative agent of white-nose syndrome, a fungal disease that has cause severe declines in several species of hibernating bats in North America. The model allowed us to estimate initial occupancy, colonization, persistence and prevalence ofPdat bat hibernacula. Additionally, utilizing the relationship between cycle threshold and pathogen load, we estimated pathogen detectability and modeled expected colony and bat pathogen loads. To assess the ability of MS-DOHM to estimate pathogen dynamics, we compared MS-DOHM’s results to those of a dynamic occupancy model and naïve detection/non-detection. MS-DOHM’s estimates of site-level pathogen presence were up to 11.9% higher than estimates from the dynamic occupancy model and 35.7% higher than naïve occupancy. Including prevalence and load in our modeling framework resulted in estimates of pathogen arrival that were two to three years earlier compared to the dynamic occupancy and naïve detection/non-detection, respectively. Compared to naïve values, MS-DOHM predicted greater pathogen loads on colonies; however, we found no difference between model estimates and naïve values of prevalence. While the model predicted no declines in site-level prevalence, there were instances where pathogen load decreased in colonies that had beenPdpositive for longer periods of time. Our findings demonstrate that accounting for pathogen load and prevalence at multiple scales changes our understanding ofPddynamics, potentially allowing earlier conservation intervention. Additionally, we found that accounting for pathogen load and prevalence within hibernacula and among individuals resulted in a better fitting model with greater predictive ability. 

ABSTRACT Bacterial pathogens remain poorly characterized in bats, especially in North America. We describe novel (and in some cases panmictic) hemoplasmas (10.1% positivity) and bartonellae (25.6% positivity) across three colonies of Mexican free-tailed bats (Tadarida brasiliensis), a partially migratory species that can seasonally travel hundreds of kilometers. Molecular analyses identified three novelCandidatushemoplasma species most similar to another novelCandidatusspecies in Neotropical molossid bats. We also detected novel hemoplasmas in sympatric cave myotis (Myotis velifer) and pallid bats (Antrozous pallidus), with sequences in the latter 96.5% related toCandidatusMycoplasma haematohominis. We identified nineBartonellagenogroups, including those in cave myotis with 96.1% similarity toCandidatusBartonella mayotimonensis. We also detectedBartonella rochalimaein migratory Mexican free-tailed bats, representing the first report of this human pathogen in the Chiroptera. Monthly sampling of migratory Mexican free-tailed bats during their North American occupancy period also revealed significant seasonality in infection for both bacterial pathogens, with prevalence increasing following spring migration, peaking in the maternity season, and declining into fall migration. The substantial diversity and seasonality of hemoplasmas and bartonellae observed here suggest that additional longitudinal, genomic, and immunological studies in bats are warranted to inform One Health approaches. IMPORTANCEBats have been intensively sampled for viruses but remain mostly understudied for bacterial pathogens. However, bacterial pathogens can have significant impacts on both human health and bat morbidity and even mortality. Hemoplasmas and bartonellae are facultative intracellular bacteria of special interest in bats, given their high prevalence and substantial genetic diversity. Surveys have also supported plausible zoonotic transmission of these bacteria from bats to humans, includingCandidatusMycoplasma haematohominis andCandidatusBartonella mayotimonensis. Greater characterization of these bacteria across global bat diversity (over 1,480 species) is therefore warranted to inform infection risks for both bats and humans, although little surveillance has thus far been conducted in North American bats. We here describe novel (and in some cases panmictic) hemoplasmas and bartonellae across three colonies of Mexican free-tailed bats and sympatric bat species. We find high genetic diversity and seasonality of these pathogens, including lineages closely related to human pathogens, such asBartonella rochalimae. 

ABSTRACT The skin microbiome is an essential line of host defense against pathogens, yet our understanding of microbial communities and how they change when hosts become infected is limited. We investigated skin microbial composition in three North American bat species (Myotis lucifugus,Eptesicus fuscus, andPerimyotis subflavus) that have been impacted by the infectious disease, white-nose syndrome, caused by an invasive fungal pathogen,Pseudogymnoascus destructans. We compared bacterial and fungal composition from 154 skin swab samples and 70 environmental samples using a targeted 16S rRNA and internal transcribed spacer amplicon approach. We found that forM. lucifugus, a species that experiences high mortality from white-nose syndrome, bacterial microbiome diversity was dramatically lower whenP. destructanswas present. Key bacterial families—including those potentially involved in pathogen defense—significantly differed in abundance in bats infected withP. destructanscompared to uninfected bats. However, skin bacterial diversity was not lower inE. fuscusorP. subflavuswhenP. destructanswas present despite populations of the latter species declining sharply from white-nose syndrome. The fungal species present on bats substantially overlapped with the fungal taxa present in the environment at the site where the bat was sampled, but fungal community composition was unaffected by the presence ofP. destructansfor any of the three bat species. This species-specific alteration in bat skin bacterial microbiomes after pathogen invasion may suggest a mechanism for the severity of white-nose syndrome inM. lucifugusbut not for other bat species impacted by the disease. IMPORTANCEInherent complexities in the composition of microbiomes can often preclude investigations of microbe-associated diseases. Instead of single organisms being associated with disease, community characteristics may be more relevant. Longitudinal microbiome studies of the same individual bats as pathogens arrive and infect a population are the ideal experiment but remain logistically challenging; therefore, investigations like our approach that are able to correlate invasive pathogens to alterations within a microbiome may be the next best alternative. The results of this study potentially suggest that microbiome-host interactions may determine the likelihood of infection. However, the contrasting relationship between Pd and the bacterial microbiomes ofMyotis lucifugusandPerimyotis subflavusindicate that we are just beginning to understand how the bat microbiome interacts with a fungal invader such as Pd. 

Abstract Disease results from interactions among the host, pathogen, and environment. Inoculation trials can quantify interactions among these players and explain aspects of disease ecology to inform management in variable and dynamic natural environments. White-nose Syndrome, a disease caused by the fungal pathogen, Pseudogymnoascus destructans ( Pd ), has caused severe population declines of several bat species in North America. We conducted the first experimental infection trial on the tri-colored bat, Perimyotis subflavus , to test the effect of temperature and humidity on disease severity. We also tested the effects of temperature and humidity on fungal growth and persistence on substrates. Unexpectedly, only 37% (35/95) of bats experimentally inoculated with Pd at the start of the experiment showed any infection response or disease symptoms after 83 days of captive hibernation. There was no evidence that temperature or humidity influenced infection response. Temperature had a strong effect on fungal growth on media plates, but the influence of humidity was more variable and uncertain. Designing laboratory studies to maximize research outcomes would be beneficial given the high costs of such efforts and potential for unexpected outcomes. Understanding the influence of microclimates on host–pathogen interactions remains an important consideration for managing wildlife diseases, particularly in variable environments. 

Abstract Substantial global attention is focused on how to reduce the risk of future pandemics. Reducing this risk requires investment in prevention, preparedness, and response. Although preparedness and response have received significant focus, prevention, especially the prevention of zoonotic spillover, remains largely absent from global conversations. This oversight is due in part to the lack of a clear definition of prevention and lack of guidance on how to achieve it. To address this gap, we elucidate the mechanisms linking environmental change and zoonotic spillover using spillover of viruses from bats as a case study. We identify ecological interventions that can disrupt these spillover mechanisms and propose policy frameworks for their implementation. Recognizing that pandemics originate in ecological systems, we advocate for integrating ecological approaches alongside biomedical approaches in a comprehensive and balanced pandemic prevention strategy. 

Many of the world’s most pressing issues, such as the emergence of zoonotic diseases, can only be addressed through interdisciplinary research. However, the findings of interdisciplinary research are susceptible to miscommunication among both professional and non-professional audiences due to differences in training, language, experience, and understanding. Such miscommunication contributes to the misunderstanding of key concepts or processes and hinders the development of effective research agendas and public policy. These misunderstandings can also provoke unnecessary fear in the public and have devastating effects for wildlife conservation. For example, inaccurate communication and subsequent misunderstanding of the potential associations between certain bats and zoonoses has led to persecution of diverse bats worldwide and even government calls to cull them. Here, we identify four types of miscommunication driven by the use of terminology regarding bats and the emergence of zoonotic diseases that we have categorized based on their root causes: (1) incorrect or overly broad use of terms; (2) terms that have unstable usage within a discipline, or different usages among disciplines; (3) terms that are used correctly but spark incorrect inferences about biological processes or significance in the audience; (4) incorrect inference drawn from the evidence presented. We illustrate each type of miscommunication with commonly misused or misinterpreted terms, providing a definition, caveats and common misconceptions, and suggest alternatives as appropriate. While we focus on terms specific to bats and disease ecology, we present a more general framework for addressing miscommunication that can be applied to other topics and disciplines to facilitate more effective research, problem-solving, and public policy. 

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.