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Over the past two decades, research on bat-associated microbes such as viruses, bacteria and fungi has dramatically increased. Here, we synthesize themes from a conference symposium focused on advances in the research of bats and their microbes, including physiological, immunological, ecological and epidemiological research that has improved our understanding of bat infection dynamics at multiple biological scales. We first present metrics for measuring individual bat responses to infection and challenges associated with using these metrics. We next discuss infection dynamics within bat populations of the same species, before introducing complexities that arise in multi-species communities of bats, humans and/or livestock. Finally, we outline critical gaps and opportunities for future interdisciplinary work on topics involving bats and their microbes.
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Quirópteros , Humanos , Animais , GadoRESUMO
A novel Hendra virus variant, genotype 2, was recently discovered in a horse that died after acute illness and in Pteropus flying fox tissues in Australia. We detected the variant in flying fox urine, the pathway relevant for spillover, supporting an expanded geographic range of Hendra virus risk to horses and humans.
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Quirópteros , Vírus Hendra , Infecções por Henipavirus , Animais , Austrália/epidemiologia , Vírus Hendra/genética , Infecções por Henipavirus/epidemiologia , Infecções por Henipavirus/veterinária , CavalosRESUMO
Models of host-pathogen interactions help to explain infection dynamics in wildlife populations and to predict and mitigate the risk of zoonotic spillover. Insights from models inherently depend on the way contacts between hosts are modelled, and crucially, how transmission scales with animal density. Bats are important reservoirs of zoonotic disease and are among the most gregarious of all mammals. Their population structures can be highly heterogeneous, underpinned by ecological processes across different scales, complicating assumptions regarding the nature of contacts and transmission. Although models commonly parameterise transmission using metrics of total abundance, whether this is an ecologically representative approximation of host-pathogen interactions is not routinely evaluated. We collected a 13-month dataset of tree-roosting Pteropus spp. from 2,522 spatially referenced trees across eight roosts to empirically evaluate the relationship between total roost abundance and tree-level measures of abundance and density-the scale most likely to be relevant for virus transmission. We also evaluate whether roost features at different scales (roost level, subplot level, tree level) are predictive of these local density dynamics. Roost-level features were not representative of tree-level abundance (bats per tree) or tree-level density (bats per m2 or m3 ), with roost-level models explaining minimal variation in tree-level measures. Total roost abundance itself was either not a significant predictor (tree-level 3D density) or only weakly predictive (tree-level abundance). This indicates that basic measures, such as total abundance of bats in a roost, may not provide adequate approximations for population dynamics at scales relevant for transmission, and that alternative measures are needed to compare transmission potential between roosts. From the best candidate models, the strongest predictor of local population structure was tree density within roosts, where roosts with low tree density had a higher abundance but lower density of bats (more spacing between bats) per tree. Together, these data highlight unpredictable and counterintuitive relationships between total abundance and local density. More nuanced modelling of transmission, spread and spillover from bats likely requires alternative approaches to integrating contact structure in host-pathogen models, rather than simply modifying the transmission function.
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Quirópteros , Doenças Transmissíveis , Animais , Dinâmica Populacional , ÁrvoresRESUMO
The spatial organization of populations determines their pathogen dynamics. This is particularly important for communally roosting species, whose aggregations are often driven by the spatial structure of their environment. We develop a spatially explicit model for virus transmission within roosts of Australian tree-dwelling bats (Pteropus spp.), parameterized to reflect Hendra virus. The spatial structure of roosts mirrors three study sites, and viral transmission between groups of bats in trees was modelled as a function of distance between roost trees. Using three levels of tree density to reflect anthropogenic changes in bat habitats, we investigate the potential effects of recent ecological shifts in Australia on the dynamics of zoonotic viruses in reservoir hosts. We show that simulated infection dynamics in spatially structured roosts differ from that of mean-field models for equivalently sized populations, highlighting the importance of spatial structure in disease models of gregarious taxa. Under contrasting scenarios of flying-fox roosting structures, sparse stand structures (with fewer trees but more bats per tree) generate higher probabilities of successful outbreaks, larger and faster epidemics, and shorter virus extinction times, compared to intermediate and dense stand structures with more trees but fewer bats per tree. These observations are consistent with the greater force of infection generated by structured populations with less numerous but larger infected groups, and may flag an increased risk of pathogen spillover from these increasingly abundant roost types. Outputs from our models contribute insights into the spread of viruses in structured animal populations, like communally roosting species, as well as specific insights into Hendra virus infection dynamics and spillover risk in a situation of changing host ecology. These insights will be relevant for modelling other zoonotic viruses in wildlife reservoir hosts in response to habitat modification and changing populations, including coronaviruses like SARS-CoV-2.
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COVID-19 , Quirópteros , Vírus , Animais , Austrália , Ecossistema , SARS-CoV-2RESUMO
The prevalence and intensity of parasites in wild hosts varies across space and is a key determinant of infection risk in humans, domestic animals and threatened wildlife. Because the immune system serves as the primary barrier to infection, replication and transmission following exposure, we here consider the environmental drivers of immunity. Spatial variation in parasite pressure, abiotic and biotic conditions, and anthropogenic factors can all shape immunity across spatial scales. Identifying the most important spatial drivers of immunity could help pre-empt infectious disease risks, especially in the context of how large-scale factors such as urbanization affect defence by changing environmental conditions. We provide a synthesis of how to apply macroecological approaches to the study of ecoimmunology (i.e. macroimmunology). We first review spatial factors that could generate spatial variation in defence, highlighting the need for large-scale studies that can differentiate competing environmental predictors of immunity and detailing contexts where this approach might be favoured over small-scale experimental studies. We next conduct a systematic review of the literature to assess the frequency of spatial studies and to classify them according to taxa, immune measures, spatial replication and extent, and statistical methods. We review 210 ecoimmunology studies sampling multiple host populations. We show that whereas spatial approaches are relatively common, spatial replication is generally low and unlikely to provide sufficient environmental variation or power to differentiate competing spatial hypotheses. We also highlight statistical biases in macroimmunology, in that few studies characterize and account for spatial dependence statistically, potentially affecting inferences for the relationships between environmental conditions and immune defence. We use these findings to describe tools from geostatistics and spatial modelling that can improve inference about the associations between environmental and immunological variation. In particular, we emphasize exploratory tools that can guide spatial sampling and highlight the need for greater use of mixed-effects models that account for spatial variability while also allowing researchers to account for both individual- and habitat-level covariates. We finally discuss future research priorities for macroimmunology, including focusing on latitudinal gradients, range expansions and urbanization as being especially amenable to large-scale spatial approaches. Methodologically, we highlight critical opportunities posed by assessing spatial variation in host tolerance, using metagenomics to quantify spatial variation in parasite pressure, coupling large-scale field studies with small-scale field experiments and longitudinal approaches, and applying statistical tools from macroecology and meta-analysis to identify generalizable spatial patterns. Such work will facilitate scaling ecoimmunology from individual- to habitat-level insights about the drivers of immune defence and help predict where environmental change may most alter infectious disease risk.
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Animais Selvagens , Parasitos , Animais , Humanos , Análise EspacialRESUMO
Ecological information on wildlife reservoirs is fundamental for research targeting prevention of zoonotic infectious disease, yet basic information is lacking for many species in global hotspots of disease emergence. We provide the first estimates of synchronicity, magnitude, and timing of seasonal birthing in Mops condylurus, a putative ebolavirus host, and a co-roosting species, Mops pumilus (formerly Chaerephon pumilus). We show that population-level synchronicity of M. condylurus birthing is wide (~ 8.5 weeks) and even wider in M. pumilus (> 11 weeks). This is predicted to promote the likelihood of filovirus persistence under conditions of bi-annual birthing (two births per year). Ecological features underlying the magnitude of the birth pulse-relative female abundance (higher than expected for M. condylurus and lower for M. pumilus, based on literature) and reproductive rate (lower than expected)-will have countering effects on birthing magnitude. Species-specific models are needed to interpret how identified birth pulse attributes may interact with other features of molossid ebolavirus ecology to influence infection dynamics. As a common feature of wildlife species, and a key driver of infection dynamics, detailed information on seasonal birthing will be fundamental for future research on these species and will be informative for bat-borne zoonoses generally.
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Quirópteros , Estações do Ano , Animais , Quirópteros/virologia , Feminino , Quênia/epidemiologia , Reservatórios de Doenças/virologia , Doença pelo Vírus Ebola/epidemiologia , Ebolavirus , Parto , Zoonoses/virologiaRESUMO
Simultaneous use of domestic spaces by humans and wildlife is little understood, despite global ubiquity, and can create an interface for human exposure to wildlife pathogens. Bats are a pervasive synanthropic taxon and are associated with several pathogens that can spill over and cause disease in humans. Urbanization has destroyed much natural bat habitat and, in response, many species increasingly use buildings as roosts. The purpose of this study was to characterize human interactions with bats in shared buildings to assess potential for human exposure to and spillover of bat-borne pathogens. We surveyed 102 people living and working in buildings used as bat roosts in Taita-Taveta county, Kenya between 2021 and 2023. We characterized and quantified the duration, intensity, and frequency of human-bat interactions occurring in this common domestic setting. Survey respondents reported living with bats in buildings year-round, with cohabitation occurring consistently for at least 10 years in 38% of cases. Human contact with bats occurred primarily through direct and indirect routes, including exposure to excrement (90% of respondents), and direct touching of bats (39% of respondents). Indirect contacts most often occurred daily, and direct contacts most often occurred yearly. Domestic animal consumption of bats was also reported (16% of respondents). We demonstrate that shared building use by bats and humans in rural Kenya leads to prolonged, frequent, and sometimes intense interactions between bats and humans, consistent with interfaces that can facilitate exposure to bat pathogens and subsequent spillover. Identifying and understanding the settings and practices that may lead to zoonotic pathogen spillover is of great global importance for developing countermeasures, and this study establishes bat roosts in buildings as such a setting.
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Quirópteros , Animais , Humanos , Quênia/epidemiologia , Zoonoses , Inquéritos e Questionários , EcossistemaRESUMO
Synanthropic bats live in close proximity to humans and domestic animals, creating opportunities for potential pathogen spillover. We explored environmental correlates of occurrence for a widely distributed synanthropic African bat, Mops pumilus-a species associated with potential zoonotic viruses-and estimated current and future environmental suitability in the Taita Hills region and surrounding plains in Taita-Taveta County in southeast Kenya. To project future environmental suitability, we used four Coupled Model Intercomparison Project Phase 6 general circulation models that capture temperature and precipitation changes for East Africa. The models were parameterized with empirical capture data of M. pumilus collected from 2016 to 2023, combined with satellite-based vegetation, topographic, and climatic data to identify responses to environmental factors. The strongest drivers for current environmental suitability for M. pumilus were short distance to rivers, higher precipitation during the driest months, sparse vegetation-often related to urban areas-and low yearly temperature variation. To predict current and future areas suitable for M. pumilus, we created ensemble niche models, which yielded excellent predictive accuracies. Current suitable environments were located southward from the central and southern Taita Hills and surrounding plains, overlapping with urban centers with the highest human population densities in the area. Future projections for 2050 indicated a moderate increase in suitability range in the southern portion of the region and surrounding plains in human-dominated areas; however, projections for 2090 showed a slight contraction of environmental suitability for M. pumilus, potentially due to the negative impact of increased temperatures. These results show how environmental changes are likely to impact the human exposure risk of bat-borne pathogens and could help public health officials develop strategies to prevent these risks in Taita-Taveta County, Kenya, and other parts of Africa.
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Many wildlife species are synanthropic and use structures built by humans, creating a high-risk interface for human-wildlife conflict and zoonotic pathogen spillover. However, studies that investigate features of urbanizing areas that attract or repel wildlife are currently lacking. We surveyed 85 buildings used by bats and 172 neighbouring buildings unused by bats (controls) in southeastern Kenya during 2021 and 2022 and evaluated the role of microclimate and structural attributes in building selection. We identified eight bat species using buildings, with over 25% of building roosts used concurrently by multiple species. Bats selected taller cement-walled buildings with higher water vapour pressure and lower presence of permanent human occupants. However, roost selection criteria differed across the most common bat species: molossids selected structures like those identified by our main dataset whereas Cardioderma cor selected buildings with lower presence of permanent human occupants. Our results show that roost selection of synanthropic bat species is based on specific buildings attributes. Further, selection criteria that facilitate bat use of buildings are not homogeneous across species. These results provide information on the general mechanisms of bat-human contact in rural settings, as well as specific information on roost selection for synanthropic bats in urbanizing Africa.
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The black flying fox (Pteropus alecto) is a natural reservoir for Hendra virus, a paramyxovirus that causes fatal infections in humans and horses in Australia. Increased excretion of Hendra virus by flying foxes has been hypothesized to be associated with physiological or energetic stress in the reservoir hosts. The objective of this study was to explore the leukocyte profiles of wild-caught P. alecto, with a focus on describing the morphology of each cell type to facilitate identification for clinical purposes and future virus spillover research. To this end, we have created an atlas of images displaying the commonly observed morphological variations across each cell type. We provide quantitative and morphological information regarding the leukocyte profiles in bats captured at two roost sites located in Redcliffe and Toowoomba, Queensland, Australia, over the course of two years. We examined the morphology of leukocytes, platelets, and erythrocytes of P. alecto using cytochemical staining and characterization of blood films through light microscopy. Leukocyte profiles were broadly consistent with previous studies of P. alecto and other Pteropus species. A small proportion of individual samples presented evidence of hemoparasitic infection or leukocyte morphological traits that are relevant for future research on bat health, including unique large granular lymphocytes. Considering hematology is done by visual inspection of blood smears, examples of the varied cell morphologies are included as a visual guide. To the best of our knowledge, this study provides the first qualitative assessment of P. alecto leukocytes, as well as the first set of published hematology reference images for this species.
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Quirópteros , Leucócitos , Animais , Quirópteros/imunologia , Vírus Hendra , QueenslandRESUMO
Fruit bats (Family: Pteropodidae) are animals of great ecological and economic importance, yet their populations are threatened by ongoing habitat loss and human persecution. A lack of ecological knowledge for the vast majority of Pteropodid species presents additional challenges for their conservation and management.In Australia, populations of flying-fox species (Genus: Pteropus) are declining and management approaches are highly contentious. Australian flying-fox roosts are exposed to management regimes involving habitat modification, through human-wildlife conflict management policies, or vegetation restoration programs. Details on the fine-scale roosting ecology of flying-foxes are not sufficiently known to provide evidence-based guidance for these regimes, and the impact on flying-foxes of these habitat modifications is poorly understood.We seek to identify and test commonly held understandings about the roosting ecology of Australian flying-foxes to inform practical recommendations and guide and refine management practices at flying-fox roosts.We identify 31 statements relevant to understanding of flying-fox roosting structure and synthesize these in the context of existing literature. We then contribute a contemporary, fine-scale dataset on within-roost structure to further evaluate 11 of these statements. The new dataset encompasses 13-monthly repeat measures from 2,522 spatially referenced roost trees across eight sites in southeastern Queensland and northeastern New South Wales.We show evidence of sympatry and indirect competition between species, including spatial segregation of black and grey-headed flying-foxes within roosts and seasonal displacement of both species by little red flying-foxes. We demonstrate roost-specific annual trends in occupancy and abundance and provide updated demographic information including the spatial and temporal distributions of males and females within roosts.Insights from our systematic and quantitative study will be important to guide evidence-based recommendations on restoration and management and will be crucial for the implementation of priority recovery actions for the preservation of these species in the future.
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Dose is the nexus between exposure and all upstream processes that determine pathogen pressure, and is thereby an important element underlying disease dynamics. Understanding the relationship between dose and disease is particularly important in the context of spillover, where nonlinearities in the dose-response could determine the likelihood of transmission. There is a need to explore dose-response models for directly transmitted and zoonotic pathogens, and how these interactions integrate within-host factors to consider, for example, heterogeneity in host susceptibility and dose-dependent antagonism. Here, we review the dose-response literature and discuss the unique role dose-response models have to play in understanding and predicting spillover events. We present a re-analysis of dose-response experiments for two important zoonotic pathogens (Middle East respiratory syndrome coronavirus and Nipah virus), to exemplify potential difficulties in differentiating between appropriate models with small exposure experiment datasets. We also discuss the data requirements needed for robust selection between dose-response models. We then suggest how these processes could be modelled to gain more realistic predictions of zoonotic transmission outcomes and highlight the exciting opportunities that could arise with increased collaboration between the virology and epidemiology disciplines. This article is part of the theme issue 'Dynamic and integrative approaches to understanding pathogen spillover'.
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Infecções por Coronavirus/transmissão , Reservatórios de Doenças/virologia , Meio Ambiente , Infecções por Henipavirus/transmissão , Interações Hospedeiro-Patógeno , Coronavírus da Síndrome Respiratória do Oriente Médio/fisiologia , Vírus Nipah/fisiologia , Animais , Animais Selvagens , HumanosRESUMO
Fire is a key process in eucalypt communities, exerting a strong influence on the composition, structure and functioning of forests. Much of the research on the fire response of temperate, wet-sclerophyll trees in Australia comes from Victoria, where the dominant eucalypt is Eucalyptus regnans. In contrast, central and northern Tasmanian forests, dominated by Eucalyptus delegatensis, are relatively understudied. There is a need to determine whether Tasmanian wet-sclerophyll forests, though the same forest type in name, are functionally different in floristics and response to fire. Here we document the forest community response to a natural wildfire event in Tasmania-using opportunistic before/after control/impact (BACI) data from pre-existing monitoring plots. Uniting pre- and post-fire floristic data, we quantified mortality and regeneration of eucalypt, acacia and other dominant tree species, and tree ferns, Dicksonia antarctica, in response to wildfire. We also evaluated the density of eucalypt and acacia seedling establishment between burnt and unburnt forests, and quantified faunal responses to fire. Despite moderate-to-high intensity burning in patches across the plot, mortality of eucalypts, acacias and tree ferns due to fire were low. By contrast, fire-sensitive rainforest species showed low survival, though were able to persist in unburnt refugia. Eucalypt and acacia seedling regeneration was high in the burnt plot, suggesting that E. delegatensis forests regenerate without stand-replacing fire events. This contrasts to Victorian E. regnans forests, whose persistence is dependent on high-severity stand-replacing events. We also found some group-specific avifaunal and invertebrate responses to the fire event, which are broadly reflective of responses documented in other Victorian-based studies. Our results have implications for Tasmanian wet-forest silvicultural practices, which are based on the principle of stand-replacement after fire. The broader relevance of this work to forest ecology is in demonstrating the serendipitous opportunities that can arise with baseline monitoring plots.