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Species differ in vulnerability to anthropogenic land use changes. Knowledge of the mechanisms driving differential sensitivity can inform conservation strategies but is generally lacking for species‐rich taxa in the tropics. The diverse bat fauna of Southeast Asia is threatened by rapid loss of forest and expanding agricultural activities, but the associations between species, traits, vulnerability to agriculture, and the underlying drivers have yet to be elucidated. We studied the responses of speciose insectivorous bat assemblages to robusta coffee cultivation in Sumatra, Indonesia. We compared abundance, species richness, and assemblage structures of bats between forests and coffee farms based on trapping data and evaluated the influence of vegetation complexity on assemblage composition and species‐level reactions. Bat abundance and species richness were significantly lower in coffee farms than in forests. Bat assemblage structure differed between land uses, and the overall variation can be largely explained by vegetation simplification. Species sensitive to coffee agriculture were associated with more complex vegetation structure, whereas tolerant species were associated with simpler vegetation structure. Sensitive and tolerant species differed in the type, frequency, and bandwidth of echolocation calls and roost use. Species sensitive to coffee use broadband and high‐pitched frequency‐modulated calls, which are efficient at detecting insects in complex vegetation, and roost in plant structures that may be lost as vegetation is simplified. In contrast, tolerant species used lower pitched constant‐frequency calls and roost in caves. We advocate for greater use of trait analyses in studies seeking to clarify the influence of agriculture on diverse tropical bat faunas. Abstract in Indonesian is available with online material.

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.

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)., Limited collaboration between bat ecologists and disease researchers has precluded integrative research on disease emergence. These historical silos are now challenged by the emergence of SARS-CoV-2, which threatens both human and bat health. This Perspective article maintains that interdisciplinary research can be accelerated when disparate domains address common, foundational causes.

The iconic African baobab tree (Adansonia digitata) has &ldquo, chiropterophilous&rdquo, flowers that are adapted for pollination by fruit bats. Although bat pollination of baobabs has been documented in east and west Africa, it has not been confirmed in southern Africa where it has been suggested that hawk moths (Nephele comma) may also be involved in baobab pollination. We used a citizen science approach to monitor baobab tree and flower visitors from dusk till midnight at 23 individual baobab trees over 27 nights during the flowering seasons (November&ndash, December) of 2016 and 2017 in northern South Africa and southern Zimbabwe (about 1650 visitors). Insect visitors frequently visited baobab flowers, including hawk moths, but, with one exception in southeastern Zimbabwe, no fruit bats visited flowers. Citizen science enabled us to substantiate preliminary conclusions about the relative importance of moth versus bat pollination of baobabs in southern Africa, with important implications for resource management.

Biosphere reserves, designated under The United Nations Education, Scientific and Cultural Organization&rsquo, s (UNESCO) Man and Biosphere Programme, aim to sustainably integrate protected areas into the biological and economic landscape around them by buffering strictly protected habitats with zones of limited use. However, the effectiveness of biosphere reserves and the contribution of the different zones of use to protection is poorly known. We assessed the diversity and activity of bats in the Crocker Range Biosphere Reserve (CRBR) in Sabah, Malaysia, using harp traps, mist nets and acoustic surveys in each zone&mdash, core, buffer, transition and in agricultural plots outside of the reserve. We captured 30 species, bringing the known bat fauna of CRBR to 50 species, half of Borneo&rsquo, s bat species. Species composition and acoustic activity varied among zones and by foraging ensemble, with the core and buffer showing particular importance for conserving forest-dependent insectivorous bats. Frugivorous bats were found in all zones but were the most abundant and most species-rich ensemble within agricultural sites. Although sampling was limited, bat diversity and activity was low in the transition zone compared to other zones, indicating potential for management practices that increase food availability and enhance biodiversity value. We conclude that, collectively, the zones of the CRBR effectively protect diversity, but the value of the transition zone can be improved.

Letter to the Editor COVID-19 has spread around the globe, with massive impacts on global human health, national economies and conservation activities. In the timely editorial about conservation in the maelstrom of COVID-19, Evans et al. (2020) urged the conservation community to collaborate with other relevant sectors of society in the search for solutions to the challenges posed by the current pandemic, as well as future zoonotic outbreaks. Considering the association of COVID 19 with bats (Zhou et al., 2020), bat conservationists will undoubtedly be key actors in this dialogue, and thus an action plan on how best to adjust bat conservation to this new reality, alongside a transdisciplinary research agenda, are clear priorities info:eu-repo/semantics/publishedVersion

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.

Human-wildlife conflicts pose a growing threat to many species worldwide and require increasingly innovative and multi-disciplinary resolutions. Because of their apparent simplicity and political appeal, lethal approaches like culling are often favoured, decisions to cull are typically poorly supported by scientific evidence and the limitations and drawbacks of culls minimised. As natural habitats decline and fruit crop production expands, fruit-eating bats in the Old World (family Pteropodidae) are increasingly in conflict with fruit farmers. This conflict is exemplified on Mauritius where the government has implemented two mass culls of a threatened flying fox (Pteropus niger) since 2015 in response to fruit-grower concerns. The culls and illegal hunting reduced the bat population by >50%. In this context, we sought to investigate the ecological role and service provided by the targeted flying fox through seed dissemination to gauge what may be lost as the species becomes rarer or extinct. We randomly sampled the woody native community in six of the best-preserved moist-to-wet native forests of Mauritius using 90 plots of 100 m2 each and identified and measured the stem size of all woody plants ≥1 cm in diameter. Species were classified by whether their fruits occur in the diet of the flying fox in an exclusive, confirmed or likely manner and we assumed that fruit consumption is equivalent to potential seed dissemination. The relative importance of these three categories to the total woody plant community was then quantified as the proportion of species richness, stem density and basal area (as a surrogate of biomass) that they represent. We also investigated whether the main traits of species (seed size, fruit size, and maximum stem diameter) vary among bat-dispersal categories and differ from those of species whose fruits are not currently known to be eaten by the flying fox. On average, although about a quarter of the native woody species (24.6%) have fruits confirmed as eaten and seeds dispersed by the flying fox, these species comprise about half (53.1%) of the stems sampled and the majority (63.1%) of the basal area of native woody plant in the island’s native forests. About half of that latter biomass figure comprises species for which the flying fox is the exclusive native vertebrate frugivore and seed disperser. Plants disseminated by the flying fox are typically large trees with large fruit and seeds. These trees are often key components of the canopy, therefore fulfilling structural engineer roles that provide resources and conditions for the survival of many forest species. The flying fox plays a disproportionally large ecological role in maintaining forest structure and biodiversity in the long-term. Consequently, lethal approaches to the conflict with fruit-farmers threaten not only an endangered species, but ecological processes central to the viability of native forests. Our findings highlight the importance of including the ecological costs of culling in decision-making processes intended to resolve human-wildlife conflicts.

Open-source species locality data are widely used in species distribution modeling but may be spatially biased by uneven sampling effort across a species' range. Spatial biases may vary across ecological trait groups if traits affect associations with landscape features and capture probability. Furthermore, spatial biases may change across time as research priorities, funding, and methodologies change, which may confound modeling of temporal changes in distributions. We used locality records from 93 bat species from the Global Biodiversity Information Facility to characterize the differential contribution of bias variables to spatial bias and how contribution varied across ecological trait groups. Next, we examined how historical changes in protected area proliferation, economic development, and sampling method advancement affected protected area and university biases. Roosting and foraging traits influenced spatial bias, but distance to protected areas was the greatest contributor to spatial sampling bias in a pooled model and 8 out of 10 ecological trait group models. Over time, distance to protected areas significantly decreased following protected area proliferation, but economic improvement did not influence distance to universities. Sampling method advancements increased protected area bias for two out of three foraging groups. Although sampling effort has increased over time, effort is becoming more biased towards protected areas, which may not encompass the entirety of species' ranges or allow for equal sampling across taxa. Characterizing spatial bias differences among species and across time clarifies underlying causes of spatial bias, information that can be leveraged to improve spatial bias correction.

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.

Bats in temperate and subtropical regions typically synchronize birth of a single young with peaks in resource availability driven by local climate patterns. In tropical rain forest, insects are available throughout the year, potentially allowing departures from seasonal monoestry. However, reproductive energy budgets may be constrained by the cost of commuting to foraging grounds from distant roosts. To test these hypotheses, we simultaneously tracked female reproductive activity of 11 insectivorous bat species, insect biomass, and local weather variables for 20 months in a Malaysian rain forest. Five species roost in forest structures and hence have low commuting costs, whereas six species depend on caves, which are limited in the landscape, and are presumed to incur higher commuting costs to foraging sites. Monthly insect biomass was positively correlated with monthly rainfall, and there was a significant relationship between insect biomass and lactation in cave-roosting but not forest-roosting species. Cave-roosting species were seasonally monoestrus, with parturition confined to a two-month period, whereas in forest-roosting species, pregnancy and lactation were recorded throughout the year. Our results suggest that the energetic costs of commuting from roosts to foraging grounds shape annual reproductive patterns in tropical rain forest insectivorous bats. Ongoing changes in forest landscapes are likely to increase these costs for cave-roosting bats, further restricting reproductive opportunities. Climate change is projected to influence the timing of rainfall events in many tropical habitats, which may disrupt relationships between rainfall, insect biomass, and bat reproductive timing, further compromising reproductive success.

Arid environments are characterized by resource pulses that cause spatio-temporal variability in species abundance, which can make population assessments difficult. Mobile acoustic methods may improve survey success by maximizing geographic extent, characterizing landscape distribution patterns, and improving encounter rates. Bats exemplify survey challenges in arid environments as they are highly mobile and aggregate around spatio-temporal resource hotspots. We compared bat detection success of stationary acoustic methods to that of mobile acoustic transects. In a semi-arid landscape, we recorded bat echolocation calls and compared three different sampling methods along the same 24 km route: a driven transect; a set of five, permanent ten-minute point counts; and a set of point counts at nightly randomized locations. The effect of method on the number of bat passes was analyzed using a bootstrapped generalized linear mixed effect model. The mean number of passes for the mobile method was 2.14 (CI: 1.45–2.99) and 0.98 (CI: 0.77–1.21) for the pooled stationary methods. We suggest that driven transects more effectively measure bat activity in arid and open landscapes. Testing of novel survey methods in arid environments is vital to conservation success as climate change increases the extent of these biomes and the variability of resource pulses.

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 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.

Cave ecosystems are subterranean biodiversity hotspots, but limited knowledge of the distribution of diversity among caves hampers their conservation. Surveys of surrogate taxa (e.g., keystone species) can identify hotspots of biodiversity when knowledge about an ecosystem is lacking. Bats are keystone species in cave ecosystems because their guano is the primary energy source supporting diverse assemblages of cave-dependent wildlife. However, directly measuring bat diversity is time-consuming and requires expert knowledge; instead, we suggest the use of correlates of bat diversity that can be derived from readily accessible data (e.g., land-use maps) and straightforward methods not requiring expert knowledge (e.g., cave surveys, interviews) as a foundation for prioritizing caves. To identify easily measurable correlates of bat diversity, we compared assemblage composition and species abundances of 21 bat species captured in 56 caves on Bohol Island, Philippines, along gradients in environmental factors and human disturbance. Model- and distance-based methods indicated that surface-level disturbance (i.e., percent non-forested habitat, degree of urbanization and road development) along with cave complexity (i.e., available roosting area, structural heterogeneity, number of entrances and temperature range) were the most influential factors governing cave-roosting bat assemblages, thus representing correlates of bat diversity. Prioritization schemes based on these correlates select combinations of caves with greater species richness than both random selection and selection of caves based on observed richness from intensive bat surveys. The use of easy-to-measure environmental and disturbance correlates of bat diversity is an effective tool to prioritize caves to protect cave-roosting bats and the cave-dependent wildlife they support.

Ecological thresholds represent a critical tipping point along an environmental gradient that, once breached, can have irreversible consequences for species persistence and assemblage structure. Thresholds can also be used to identify species with the greatest sensitivity to environmental changes. Bats are keystone species yet are under pressure from human disturbances, specifically landscape and cave disturbances (i.e., reduced forest cover, urbanization, hunting, tourism). We compared bat assemblages across environmental and disturbance gradients measured at 56 caves in the Philippines to identify species-specific thresholds and assess congruence among species responses. All species exhibited significant responses to one or more gradients, with 84% responding to more than one gradient. Yet mixed responses of sensitivity to some gradients but tolerance to others hindered identification of assemblage thresholds to all gradients except landscape disturbance. However, we identified credible indicator species that exhibit distinct thresholds to specific gradients and tested for differences in ecological and morphological traits between species groups with shared responses (i.e., negative or positive). Few traits were useful for discriminating the direction of a species response, with some exceptions. Species that responded positively to increased landscape disturbance and hunting had greater body mass, whereas species that responded negatively to mining emitted higher peak call frequencies.

Flying foxes provide critical ecosystem services by pollinating and disseminating diverse plant species. Yet, they face intensifying threats, particularly on islands. The situation is epitomized by the Indian Ocean island of Mauritius. In December 2016, the Mauritian government implemented the second mass cull of a threatened, endemic flying fox species, Pteropus niger (see the left photo), in 2 years. Government figures suggest that at least 45% of the overall P. niger population of just over 90,000 individuals were culled during the two campaigns; illegal killing and incidental mortality of pups during the culls raise likely losses to over 50%. The dire situation of island flying foxes worldwide calls for effective, science-based conservation strategies to prevent further loss of biodiversity and function.

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.

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.

Summary 1. Species richness is a state variable of some interest in monitoring programmes but raw species counts are often biased due to imperfect species detectability. Therefore, monitoring programmes should quantify detectability for target taxa to assess whether it varies over temporal or spatial scales. We assessed the potential for tropical bat monitoring programmes to reliably estimate trends in species richness. 2. Using data from 25 bat assemblages from the Old and New World tropics, we estimated detectability for all species in an assemblage (mean proportion of species detected per sampling plot) and for individual species (species-specific detectability). We further assessed how these estimates of detectability were affected by external sources of variation relating to time, space, survey effort and biological traits. 3. The mean proportion of species detected across 96 sampling plots was estimated at 0AE76 (range 0AE57–1AE00) and was significantly greater for phytophagous than for animalivorous species. Species

International audience; Bats are ecologically important mammals in tropical ecosystems; however, their populations face numerous environmental threats related to climate change, habitat loss, fragmentation, hunting, and emerging diseases. Thus, there is a pressing need to develop and implement large-scale networks to monitor trends in bat populations over extended time periods. Using data from a range of Neotropical and Paleotropical bat assemblages, we assessed the ability for long-term monitoring programs to reliably detect temporal trends in species abundance. We explored the magnitude of within-site temporal variation in abundance and evaluated the statistical power of a suite of different sampling designs for several different bat species and ensembles. Despite pronounced temporal variation in abundance of most tropical bat species, power simulations suggest that long-term monitoring programs (>= 20 years) can detect population trends of 5% per year or more with adequate statistical power (>= 0.9). However, shorter monitoring programs (