Ecological countermeasures to prevent pathogen spillover and subsequent pandemics.

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.

Future directions for One Health research: Regional and sectoral gaps.

Implementation of a One Health approach varies considerably between different geographical regions and remains challenging to implement without greater inclusivity of different disciplinary capacity and expertise. We performed comparative analyses of abstracts presented at the 1st World One Health Congress (WOHC 2011) and 6th WOHC (2020) to explore and describe the evolving demographics and disciplinary scope of One Health research. We classified abstracts into six One Health research categories and twenty-three subcategories. We also recorded corresponding authors' country and regional affiliation as well as study country (i.e., the country in which the research was conducted) to explore potential asymmetries between funding recipients and study subjects. The WOHC has seen a significant expansion in participation over the last 10 years. The numbers of abstracts accepted to the Congress increased threefold over the last decade (i.e., 302 abstracts in 2010, and 932 abstracts in 2020). At both Congresses, "Disease Surveillance" accounted for the largest proportion (105/302 (35%) and 335/932 (36%) in 2010 and 2020, respectively) of all abstracts accepted. However, "Environmental and Ecological Issues" (33/302 (10%) and 94/932 (11%)), and "Sustainable Food Systems" (19/302 (6%) and 44/932 (4%)) were less well-represented categories of One Health research in both 1st and 6th WOHC respectively. In contrast, "Antimicrobial Resistance" related research increased substantially over time (4/302 (1%) in 2011) and (119/932 (13%) in 2020). There were also differences in the type of research by authors based in "Very High Human Development" index countries compared to "Medium and Low Human Development. "Public Policy" dominated the former, whereas "Disease Surveillance" dominated the latter, suggesting potential regional differences regarding One Health research priorities. The results of the study highlight potential regional gaps and differences in One Health research priorities, with respect to emphasis on operational (surveillance) versus strategic (policy) One Health activities.

Using drivers and transmission pathways to identify SARS-like coronavirus spillover risk hotspots.

The emergence of SARS-like coronaviruses is a multi-stage process from wildlife reservoirs to people. Here we characterize multiple drivers-landscape change, host distribution, and human exposure-associated with the risk of spillover of zoonotic SARS-like coronaviruses to help inform surveillance and mitigation activities. We consider direct and indirect transmission pathways by modeling four scenarios with livestock and mammalian wildlife as potential and known reservoirs before examining how access to healthcare varies within clusters and scenarios. We found 19 clusters with differing risk factor contributions within a single country (N = 9) or transboundary (N = 10). High-risk areas were mainly closer (11-20%) rather than far ( < 1%) from healthcare. Areas far from healthcare reveal healthcare access inequalities, especially Scenario 3, which includes wild mammals and not livestock as secondary hosts. China (N = 2) and Indonesia (N = 1) had clusters with the highest risk. Our findings can help stakeholders in land use planning, integrating healthcare implementation and One Health actions.

Present and future distribution of bat hosts of sarbecoviruses: implications for conservation and public health.

Global changes in response to human encroachment into natural habitats and carbon emissions are driving the biodiversity extinction crisis and increasing disease emergence risk. Host distributions are one critical component to identify areas at risk of viral spillover, and bats act as reservoirs of diverse viruses. We developed a reproducible ecological niche modelling pipeline for bat hosts of SARS-like viruses (subgenus Sarbecovirus), given that several closely related viruses have been discovered and sarbecovirus-host interactions have gained attention since SARS-CoV-2 emergence. We assessed sampling biases and modelled current distributions of bats based on climate and landscape relationships and project future scenarios for host hotspots. The most important predictors of species distributions were temperature seasonality and cave availability. We identified concentrated host hotspots in Myanmar and projected range contractions for most species by 2100. Our projections indicate hotspots will shift east in Southeast Asia in locations greater than 2°C hotter in a fossil-fuelled development future. Hotspot shifts have implications for conservation and public health, as loss of population connectivity can lead to local extinctions, and remaining hotspots may concentrate near human populations.

ChiroVox: a public library of bat calls.

Recordings of bat echolocation and social calls are used for many research purposes from ecological studies to taxonomy. Effective use of these relies on identification of species from the recordings, but comparative recordings or detailed call descriptions to support identification are often lacking for areas with high biodiversity. The ChiroVox website (https://www.chirovox.org) was created to facilitate the sharing of bat sound recordings together with their metadata, including biodiversity data and recording circumstances. To date, more than 30 researchers have contributed over 3,900 recordings of nearly 200 species, making ChiroVox the largest open-access bat call library currently available. Each recording has a unique identifier that can be cited in publications; hence the acoustic analyses are repeatable. Most of the recordings available through the website are from bats whose species identities are confirmed, so they can be used to determine species in recordings where the bats were not captured or could not be identified. We hope that with the help of the bat researcher community, the website will grow rapidly and will serve as a solid source for bat acoustic research and monitoring.

Setting the Terms for Zoonotic Diseases: Effective Communication for Research, Conservation, and Public Policy.

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.

Common ground: The foundation of interdisciplinary research on bat disease emergence.

Human perturbation of natural systems is accelerating the emergence of infectious diseases, mandating integration of disease and ecological research. Bats have been associated with recent zoonoses, but our bibliometric analysis of coauthor relationships identified a separation of bat ecologists and infectious disease researchers with few cross-disciplinary relationships. Of 5,645 papers, true interdisciplinary collaborations occurred primarily in research focused on White Nose Syndrome (WNS). This finding is important because it illustrates how research with outcomes favoring both bat conservation and disease mitigation promotes domain integration and network connectivity. We advocate for increased engagement between ecology and infectious researchers to address such common causes and suggest that efforts focus on leveraging existing activities, building interdisciplinary projects, and networking individuals and networks to integrate domains and coordinate resources. We provide specific opportunities for pursuing these strategies through the Bat One Health Research Network (BOHRN).

Possibility for reverse zoonotic transmission of SARS-CoV-2 to free-ranging wildlife: A case study of bats.

The COVID-19 pandemic highlights the substantial public health, economic, and societal consequences of virus spillover from a wildlife reservoir. Widespread human transmission of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) also presents a new set of challenges when considering viral spillover from people to naïve wildlife and other animal populations. The establishment of new wildlife reservoirs for SARS-CoV-2 would further complicate public health control measures and could lead to wildlife health and conservation impacts. Given the likely bat origin of SARS-CoV-2 and related beta-coronaviruses (ß-CoVs), free-ranging bats are a key group of concern for spillover from humans back to wildlife. Here, we review the diversity and natural host range of ß-CoVs in bats and examine the risk of humans inadvertently infecting free-ranging bats with SARS-CoV-2. Our review of the global distribution and host range of ß-CoV evolutionary lineages suggests that 40+ species of temperate-zone North American bats could be immunologically naïve and susceptible to infection by SARS-CoV-2. We highlight an urgent need to proactively connect the wellbeing of human and wildlife health during the current pandemic and to implement new tools to continue wildlife research while avoiding potentially severe health and conservation impacts of SARS-CoV-2 "spilling back" into free-ranging bat populations.

A review of the major threats and challenges to global bat conservation.

Bats are an ecologically and taxonomically diverse group accounting for roughly a fifth of mammalian diversity worldwide. Many of the threats bats face (e.g., habitat loss, bushmeat hunting, and climate change) reflect the conservation challenges of our era. However, compared to other mammals and birds, we know significantly less about the population status of most bat species, which makes prioritizing and planning conservation actions challenging. Over a third of bat species assessed by the International Union for Conservation of Nature (IUCN) are considered threatened or data deficient, and well over half of the species have unknown or decreasing population trends. That equals 988 species, or 80% of bats assessed by IUCN, needing conservation or research attention. Delivering conservation to bat species will require sustained efforts to assess population status and trends and address data deficiencies. Successful bat conservation must integrate research and conservation to identify stressors and their solutions and to test the efficacy of actions to stabilize or increase populations. Global and regional networks that connect researchers, conservation practitioners, and local stakeholders to share knowledge, build capacity, and prioritize and coordinate research and conservation efforts, are vital to ensuring sustainable bat populations worldwide.

Clutter negotiating ability in an ensemble of forest interior bats is driven by body mass.

Differences in wing morphology are predicted to reflect differences in bat foraging strategies. Experimental tests of this prediction typically assess the relationship between wing morphology and a measures of flight performance on an obstacle course. However, studies have lacked measures of obstacle avoidance ability true scores, which may confound interpretation of ability across the range of presented tasks. Here, we used Rasch analysis of performance in a collision-avoidance experiment to estimate the ability of bat species to fly through vegetative clutter. We refer to this latent trait as 'clutter negotiating ability' and determined the relationships between clutter negotiating ability and wing morphology in 15 forest insectivorous bat species that forage in the densely cluttered rainforests of Malaysia. The clutter negotiating ability scores were quantified based on individual responses of each species to 11 different obstacle arrangements (four banks of vertical strings 10-60 cm apart). The tasks employed for the collision-avoidance experiment were reliable and valid, although Rasch analysis suggested that the experiment was too easy to discriminate completely among the 15 species. We found significant negative correlations between clutter negotiating ability and body mass, wingspan, wing loading and wing area but a positive significant correlation with wingtip area ratio. However, in stepwise multiple regression analyses, only body mass and wing loading were significant predictors of clutter negotiating ability. Species fell into clusters of different clutter negotiating ability, suggesting a potential mechanism for resource partitioning within the forest interior insectivorous ensemble.

Environmental and biological context modulates the physiological stress response of bats to human disturbance.

Environmental and biological context play significant roles in modulating physiological stress responses of individuals in wildlife populations yet are often overlooked when evaluating consequences of human disturbance on individual health and fitness. Furthermore, most studies gauge individual stress responses based on a single physiological biomarker, typically circulating glucocorticoid concentrations, which limits interpretation of the complex, multifaceted responses of individuals to stressors. We selected four physiological biomarkers to capture short-term and prolonged stress responses in a widespread cave-roosting bat, Hipposideros diadema, across multiple gradients of human disturbance in and around caves in the Philippines. We used conditional inference trees and random forest analysis to determine the role of environmental quality (cave complexity, available roosting area), assemblage composition (intra- and interspecific associations and species richness), and intrinsic characteristics of individuals (sex and reproductive status) in modulating responses to disturbance. Direct cave disturbance (hunting pressure and human visitation) was the primary driver of neutrophil-to-lymphocyte ratios, with lower ratios associated with increased disturbance, while context-specific factors were more important in explaining total leukocyte count, body condition, and ectoparasite load. Moreover, conditional inference trees revealed complex interactions among human disturbance and modulating factors. Cave complexity often ameliorated individual responses to human disturbance, whereas conspecific abundance often compounded responses. Our study demonstrates the importance of an integrated approach that incorporates environmental and biological context when identifying drivers of physiological responses, and that assesses responses to gradients of direct and indirect disturbance using multiple complementary biomarkers.

Microbiome Structural and Functional Interactions across Host Dietary Niche Space.

Host-associated microbiomes are integral components of host health, but microbiome community structure varies among and within hosts. Reconciling community variability with the apparent dependence of hosts on community function, and characterizing how functional divergence proceeds across niches, remains challenging. Here, through the study of gut microbiomes and diets of three insectivorous bat species we characterize how community structure is shaped by predicted functional properties of community members. We found that while host diet and microbiome community composition do not significantly relate to each other, host diet and metagenome function do, suggesting that diet directly selects metagenomic functions rather than communities. We use a novel inference framework to show how the discordance between community structure and functional variation derives from functional equivalence and is influenced by the continuum of shared and derived gene sets across microbial lineages. Our findings help clarify how metagenome community structure-function relationships contribute to deterministic processes in community assembly, and describe the basis for metagenomic differences across ecologically similar hosts.

Temporal dynamics of relative abundances and bacterial succession in chronic wound communities.

Polymicrobial bacterial infection is an important factor contributing to wound chronicity. Consequently, clinicians frequently adopt a biofilm-based wound care approach, in which wounds are treated utilizing DNA sequencing information about microbial communities. While more successful than treatment not using community information, there is little information about temporal dynamics of wound communities and optimal approaches over the course of treatment. To characterize these dynamics, temporal analysis over three sampling points was conducted for 167 chronic wounds. Across sampling intervals, wound communities from the same patients changed in composition, and most commonly shared less than 50% of observed species. There was a significant relationship between community similarity and time between sampling. Classifying wounds into state types, we found that communities frequently transitioned from Pseudomonas or Staphylococcus dominated, into a highly variable state type. Although low abundance microbial species are typically disregarded due to uncertainty of biological importance, we found that 80% of wound microbiomes included common or dominant species at subsequent time points that were in low abundance in earlier samples. Moreover, these species were often those known to frequently infect wounds. Results document compositional shifts through the course of treatment and suggest that routine consideration of low abundance species may improve biofilm-based wound care. Moreover, findings indicate that integrating ecological modeling to understand wound microbiome succession may lead to more informed therapy.

Thumb-pads up-a new species of thick-thumbed bat from Sumatra (Chiroptera: Vespertilionidae: Glischropus).

To date, three species of the genus Glischropus are recognized from the Indomalayan zoogeographic region-G. bucephalus from the Indochinese subregion, G. tylopus from the Sundaic subregion (Peninsular Thailand and Malaysia, Borneo, Sumatra, Moluccas) and G. javanus, restricted to Java. The investigation of the holotype and three topotype specimens of G. batjanus supported the view that the name was previously correctly regarded as the junior subjective synonym of G. tylopus. During review of material recently collected in southwestern Sumatra, Indonesia, one specimen of a yet undescribed species of Thick-thumbed bat was identified. G. aquilus n. sp. markedly differs from its congeners by its dark brown pelage, nearly black ear and tragus, and in skull proportions. The phylogenetic analysis based on cytb sequences also supports the specific distinctness of G. aquilus n. sp. Its discovery brings the count to 88 species of bats known from Sumatra.

Social organization and genetic structure: insights from codistributed bat populations.

The impact of ecology and social organization on genetic structure at landscape spatial scales, where gene dynamics shape evolution as well as determine susceptibility to habitat fragmentation, is poorly understood. Attempts to assess these effects must take into account the potentially confounding effects of history. We used microsatellites to compare genetic structure in seven bat species with contrasting patterns of roosting ecology and social organization, all of which are codistributed in an ancient forest habitat that has been exceptionally buffered from radical habitat shifts. Over one thousand individuals were captured at foraging sites and genotyped at polymorphic microsatellite loci. Analyses of spatially explicit genotype data revealed interspecies differences in the extent of movement and gene flow and genetic structure across continuous intact forest. Highest positive genetic structure was observed in tree-roosting taxa that roost either alone or in small groups. By comparison, a complete absence of genetic autocorrelation was noted in the cave-roosting colonial species across the study area. Our results thus reveal measurable interspecies differences in the natural limits of gene flow in an unmodified habitat, which we attribute to contrasting roosting ecology and social organization. The consequences of ecology and behaviour for gene flow have important implications for conservation. In particular, tree-roosting species characterized by lower vagility and thus gene flow will be disproportionally impacted by landscape-scale forest clearance and habitat fragmentation, which are prevalent in the study region. Our method also highlights the usefulness of rapid sampling of foraging bats for assaying genetic structure, particularly where roosting sites are not always known.

Molecular phylogeny of hipposiderid bats from Southeast Asia and evidence of cryptic diversity.

Old World leaf-nosed bats (Hipposideridae) are among the most widespread and ecologically diverse groups of insectivorous bats in the Old World tropics. However, phylogenetic relationships in Hipposideridae are poorly resolved at both the generic and species levels, and deep genetic divergence within several Southeast Asian species suggests that current taxonomy underestimates hipposiderid diversity in this region. We used mitochondrial and nuclear sequence data to conduct the first extensive molecular phylogenetic analysis of Southeast Asian hipposiderid bats. Inclusion of multiple samples per taxon allowed testing for evidence of evolutionarily distinct lineages within taxa currently defined as single species. In contrast to earlier phylogenies based on morphometrics, molecular data support monophyly of Hipposideros, but are ambiguous regarding the monophyly of Hipposideridae. With a few exceptions, molecular data also support currently recognized species groups classified by qualitative morphological characters. Widespread paraphyly and polyphyly within many currently recognized species of Hipposideros indicates that evolutionary diversity in the genus is underrepresented by current nomenclature. Comparison of available morphological and echolocation data suggest that both geographic isolation and ecological selection have contributed to the diversification of Southeast Asian hipposiderid bats.

Parallel declines in species and genetic diversity in tropical forest fragments.

The potential for parallel impacts of habitat change on multiple biodiversity levels has important conservation implications. We report on the first empirical test of the 'species-genetic diversity correlation' across co-distributed taxa with contrasting ecological traits in the context of habitat fragmentation. In a rainforest landscape undergoing conversion to oil palm, we show that depauperate species richness in fragments is mirrored by concomitant declines in population genetic diversity in the taxon predicted to be most susceptible to fragmentation. This association, not seen in the other species, relates to fragment area rather than isolation. While highlighting the over-simplification of extrapolating across taxa, we show that fragmentation presents a double jeopardy for some species. For these, conserving genetic diversity at levels of pristine forest could require sites 15-fold larger than those needed to safeguard species numbers. Importantly, however, each fragment contributes to regional species richness, with larger ones tending to contain more species.

Breaking the trade-off: rainforest bats maximize bandwidth and repetition rate of echolocation calls as they approach prey.

Both mammals and birds experience a performance trade-off between producing vocalizations with high bandwidths and at high repetition rate. Echolocating bats drastically increase repetition rate from 2-20 calls s(-1) up to about 170 calls s(-1) prior to intercepting airborne prey in order to accurately track prey movement. In turn, bandwidth drops to about 10-30 kHz for the calls of this 'final buzz'. We have now discovered that Southeast Asian rainforest bats (in the vespertilionid subfamilies Kerivoulinae and Murininae) are able to maintain high call bandwidths at very high repetition rates throughout approach to prey. Five species of Kerivoula and Phoniscus produced call bandwidths of between 78 and 170 kHz at repetition rates of 140-200 calls s(-1) and two of Murina at 80 calls s(-1). The 'typical' and distinct drop in call frequency was present in none of the seven species. This stands in striking contrast to our present view of echolocation during approach to prey in insectivorous bats, which was established largely based on European and American members of the same bat family, the Vespertilionidae. Buzz calls of Kerivoula pellucida had mean bandwidths of 170 kHz and attained maximum starting frequencies of 250 kHz which makes them the most broadband and most highly pitched tonal animal vocalization known to date. We suggest that the extreme vocal performance of the Kerivoulinae and Murininae evolved as an adaptation to echolocating and tracking arthropods in the dense rainforest understorey.

Harmonic-hopping in Wallacea's bats.

Evolutionary divergence between species is facilitated by ecological shifts, and divergence is particularly rapid when such shifts also promote assortative mating. Horseshoe bats are a diverse Old World family (Rhinolophidae) that have undergone a rapid radiation in the past 5 million years. These insectivorous bats use a predominantly pure-tone echolocation call matched to an auditory fovea (an over-representation of the pure-tone frequency in the cochlea and inferior colliculus) to detect the minute changes in echo amplitude and frequency generated when an insect flutters its wings. The emitted signal is the accentuated second harmonic of a series in which the fundamental and remaining harmonics are filtered out. Here we show that three distinct, sympatric size morphs of the large-eared horseshoe bat (Rhinolophus philippinensis) echolocate at different harmonics of the same fundamental frequency. These morphs have undergone recent genetic divergence, and this process has occurred in parallel more than once. We suggest that switching harmonics creates a discontinuity in the bats' perception of available prey that can initiate disruptive selection. Moreover, because call frequency in horseshoe bats has a dual function in resource acquisition and communication, ecological selection on frequency might lead to assortative mating and ultimately reproductive isolation and speciation, regardless of external barriers to gene flow.