Robust evidence for bats as reservoir hosts is lacking in most African virus studies: a review and call to optimize sampling and conserve bats.

Africa experiences frequent emerging disease outbreaks among humans, with bats often proposed as zoonotic pathogen hosts. We comprehensively reviewed virus-bat findings from papers published between 1978 and 2020 to evaluate the evidence that African bats are reservoir and/or bridging hosts for viruses that cause human disease. We present data from 162 papers (of 1322) with original findings on (1) numbers and species of bats sampled across bat families and the continent, (2) how bats were selected for study inclusion, (3) if bats were terminally sampled, (4) what types of ecological data, if any, were recorded and (5) which viruses were detected and with what methodology. We propose a scheme for evaluating presumed virus-host relationships by evidence type and quality, using the contrasting available evidence for Orthoebolavirus versus Orthomarburgvirus as an example. We review the wording in abstracts and discussions of all 162 papers, identifying key framing terms, how these refer to findings, and how they might contribute to people's beliefs about bats. We discuss the impact of scientific research communication on public perception and emphasize the need for strategies that minimize human-bat conflict and support bat conservation. Finally, we make recommendations for best practices that will improve virological study metadata.

Pest suppression by bats and management strategies to favour it: a global review.

Fighting insect pests is a major challenge for agriculture worldwide, and biological control and integrated pest management constitute well-recognised, cost-effective ways to prevent and overcome this problem. Bats are important arthropod predators globally and, in recent decades, an increasing number of studies have focused on the role of bats as natural enemies of agricultural pests. This review assesses the state of knowledge of the ecosystem services provided by bats as pest consumers at a global level and provides recommendations that may favour the efficiency of pest predation by bats. Through a systematic review, we assess evidence for predation, the top-down effect of bats on crops and the economic value of ecosystem services these mammals provide, describing the different methodological approaches used in a total of 66 reviewed articles and 18 agroecosystem types. We also provide a list of detailed conservation measures and management recommendations found in the scientific literature that may favour the delivery of this important ecosystem service, including actions aimed at restoring bat populations in agroecosystems. The most frequent recommendations include increasing habitat heterogeneity, providing additional roosts, and implementing laws to protect bats and reduce agrochemical use. However, very little evidence is available on the direct consequences of these practices on bat insectivory in farmland. Additionally, through a second in-depth systematic review of scientific articles focused on bat diet and, as part of the ongoing European Cost Action project CA18107, we provide a complete list of 2308 documented interactions between bat species and their respective insect pest prey. These pertain to 81 bat species belonging to 36 different genera preying upon 760 insect pests from 14 orders in agroecosystems and other habitats such as forest or urban areas. The data set is publicly available and updatable.

Newspaper Coverage and Framing of Bats, and Their Impact on Readership Engagement.

The media is a valuable pathway for transforming people's attitudes towards conservation issues. Understanding how bats are framed in the media is hence essential for bat conservation, particularly considering the recent fearmongering and misinformation about the risks posed by bats. We reviewed bat-related articles published online no later than 2019 (before the recent COVID19 pandemic), in 15 newspapers from the five most populated countries in Western Europe. We examined the extent to which bats were presented as a threat to human health and the assumed general attitudes towards bats that such articles supported. We quantified press coverage on bat conservation values and evaluated whether the country and political stance had any information bias. Finally, we assessed their terminology and, for the first time, modelled the active response from the readership based on the number of online comments. Out of 1095 articles sampled, 17% focused on bats and diseases, 53% on a range of ecological and conservation topics, and 30% only mention bats anecdotally. While most of the ecological articles did not present bats as a threat (97%), most articles focusing on diseases did so (80%). Ecosystem services were mentioned on very few occasions in both types (< 30%), and references to the economic benefits they provide were meagre (< 4%). Disease-related concepts were recurrent, and those articles that framed bats as a threat were the ones that garnered the highest number of comments. Therefore, we encourage the media to play a more proactive role in reinforcing positive conservation messaging by presenting the myriad ways in which bats contribute to safeguarding human well-being and ecosystem functioning.

Inferring genetic structure when there is little: population genetics versus genomics of the threatened bat Miniopterus schreibersii across Europe.

Despite their paramount importance in molecular ecology and conservation, genetic diversity and structure remain challenging to quantify with traditional genotyping methods. Next-generation sequencing holds great promises, but this has not been properly tested in highly mobile species. In this article, we compared microsatellite and RAD-sequencing (RAD-seq) analyses to investigate population structure in the declining bent-winged bat (Miniopterus schreibersii) across Europe. Both markers retrieved general patterns of weak range-wide differentiation, little sex-biased dispersal, and strong isolation by distance that associated with significant genetic structure between the three Mediterranean Peninsulas, which could have acted as glacial refugia. Microsatellites proved uninformative in individual-based analyses, but the resolution offered by genomic SNPs illuminated on regional substructures within several countries, with colonies sharing migrators of distinct ancestry without admixture. This finding is consistent with a marked philopatry and spatial partitioning between mating and rearing grounds in the species, which was suspected from marked-recaptured data. Our study advocates that genomic data are necessary to properly unveil the genetic footprints left by biogeographic processes and social organization in long-distant flyers, which are otherwise rapidly blurred by their high levels of gene flow.

Edge effects and vertical stratification of aerial insectivorous bats across the interface of primary-secondary Amazonian rainforest.

Edge effects, abiotic and biotic changes associated with habitat boundaries, are key drivers of community change in fragmented landscapes. Their influence is heavily modulated by matrix composition. With over half of the world's tropical forests predicted to become forest edge by the end of the century, it is paramount that conservationists gain a better understanding of how tropical biota is impacted by edge gradients. Bats comprise a large fraction of tropical mammalian fauna and are demonstrably sensitive to habitat modification. Yet, knowledge about how bat assemblages are affected by edge effects remains scarce. Capitalizing on a whole-ecosystem manipulation in the Central Amazon, the aims of this study were to i) assess the consequences of edge effects for twelve aerial insectivorous bat species across the interface of primary and secondary forest, and ii) investigate if the activity levels of these species differed between the understory and canopy and if they were modulated by distance from the edge. Acoustic surveys were conducted along four 2-km transects, each traversing equal parts of primary and ca. 30-year-old secondary forest. Five models were used to assess the changes in the relative activity of forest specialists (three species), flexible forest foragers (three species), and edge foragers (six species). Modelling results revealed limited evidence of edge effects, except for forest specialists in the understory. No significant differences in activity were found between the secondary or primary forest but almost all species exhibited pronounced vertical stratification. Previously defined bat guilds appear to hold here as our study highlights that forest bats are more edge-sensitive than edge foraging bats. The absence of pronounced edge effects and the comparable activity levels between primary and old secondary forests indicates that old secondary forest can help ameliorate the consequences of fragmentation on tropical aerial insectivorous bats.

Winter bat activity: The role of wetlands as food and drinking reservoirs under climate change.

Bat arousals during hibernation are related to rises in environmental temperature, body water loss and increasing body heat. Therefore, bats either hibernate in cold places or migrate to areas with mild winters to find water and insects to intake. During winter, insects are relatively abundant in wetlands with mild climates when low temperatures hamper insect activity in other places. However, the role of wetlands to sustain winter bat activity has never been fully assessed. To further understand bat behaviour during hibernation, we evaluated how the weather influenced hibernating bats, assessed the temperature threshold that increased bat arousals, and discussed how winter temperatures could affect bat activity under future climate change scenarios. The effects of weather and landscape composition on winter bat activity were assessed by acoustically sampling four different habitats (wetlands, rice paddies, urban areas and salt marshes) in the Ebro Delta (Spain). Our results show one of the highest winter bat foraging activities ever reported, with significantly higher activity in wetlands and urban areas. Most importantly, we found a substantial increase in bat activity triggered when nocturnal temperatures reached ca. 11 °C. By contrasting historical weather datasets, we show that, since the 1940s, there has been an increase by ca. 1.5 °C in winter maximum temperatures and a 180% increase in the number of nights with mean temperatures above 11 °C in the Ebro Delta. Temperature trends suggest that in 60-80 years, winter months will reach average temperatures of 11 °C (except maybe in January), which suggest a potential coming interruption or disappearance of bat hibernation in coastal Mediterranean habitats. This study highlights the significant role of wetlands in bat conservation under a climate change scenario as these humid areas represent one of the few remaining winter foraging habitats.

Optimizing bat bioacoustic surveys in human-modified Neotropical landscapes.

During the last decades, the use of bioacoustics as a non-invasive and cost-effective sampling method has greatly increased worldwide. For bats, acoustic surveys have long been known to complement traditional mist-netting, however, appropriate protocol guidelines are still lacking for tropical regions. Establishing the minimum sampling effort needed to detect ecological changes in bat assemblages (e.g., activity, composition, and richness) is crucial in view of workload and project cost constraints, and because detecting such changes must be reliable enough to support effective conservation management. Using one of the most comprehensive tropical bat acoustic data sets, collected in the Amazon, we assessed the minimum survey effort required to accurately assess the completeness of assemblage inventories and habitat selection in fragmented forest landscapes for aerial insectivorous bats. We evaluated a combination of 20 different temporal sampling schemes, which differed regarding number of hours per night, number of nights per site, and sampling only during the wet or dry season, or both. This was assessed under two different landscape scenarios: in primary forest fragments embedded in a matrix of secondary forest and in the same forest fragments, but after they had been re-isolated through clearing of the secondary forest. We found that the sampling effort required to achieve 90% inventory completeness varied considerably depending on the research aim and the landscape scenario evaluated, averaging ~80 and 10 nights before and after fragment re-isolation, respectively. Recording for more than 4 h per night did not result in a substantial reduction in the required number of sampling nights. Regarding the effects of habitat selection, except for assemblage composition, bat responses in terms of richness, diversity, and activity were similar across all sampling schemes after fragment re-isolation. However, before re-isolation, a minimum of four to six sampling hours per night after dusk and three to five nights of sampling per site were needed to detect significant effects that could otherwise go unnoticed. Based on our results, we propose guidelines that will aid to optimize sampling protocols for bat acoustic surveys in the Neotropics.

Quantifying and addressing the prevalence and bias of study designs in the environmental and social sciences.

Building trust in science and evidence-based decision-making depends heavily on the credibility of studies and their findings. Researchers employ many different study designs that vary in their risk of bias to evaluate the true effect of interventions or impacts. Here, we empirically quantify, on a large scale, the prevalence of different study designs and the magnitude of bias in their estimates. Randomised designs and controlled observational designs with pre-intervention sampling were used by just 23% of intervention studies in biodiversity conservation, and 36% of intervention studies in social science. We demonstrate, through pairwise within-study comparisons across 49 environmental datasets, that these types of designs usually give less biased estimates than simpler observational designs. We propose a model-based approach to combine study estimates that may suffer from different levels of study design bias, discuss the implications for evidence synthesis, and how to facilitate the use of more credible study designs.

Second capture of Promops centralis (Chiroptera) in French Guiana after 28 years of mist-netting and description of its echolocation and distress calls

la literatura científica no encontramos información muy detallada sobre especies de murciélago esquivas como las de la família Molossidae. Esta carencia condiciona y obstaculiza los esfuerzos de conservación tanto a escala local como global. El desarrollo reciente de nuevas tecnologías diseñadas específicamente para muestrear quirópteros, como los detectores de ultrasonidos pasivos o los reclamos acústicos mediante el uso de llamadas de alta frecuencia, ha incrementado nuestro conocimiento sobre su ecología y distribución. Además, ha permitido a los investigadores obtener nuevos datos que eran prácticamente imposibles de conseguir en el pasado. Llevamos a cabo una evaluación rápida de diversidad quiropterológica en la Guayana Francesa, utilizando reclamos cústicos con el objetivo de capturar especies insectívoras de vuelo alto. En este estudio, aportamos la segunda y tercera captura de Promops centralis (Chiroptera, Molossidae) para Guayana Francesa después de 28 años desde sus primeras y únicas capturas hasta ahora. Uno de los indivíduos capturados fue una hembra poslactante, el primer registro de reproducción de la especie. Aportamos (i) datos morfométricos, bioacústicos (incluyendo las llamadas de alarma típicas de la especie) y fotografías de detalles para facilitarsu identificación; y (ii) las secuencias de COI y CytB de los dos individuos (las primeras secuencias mitocondriales para la Guayana Francesa). (AU)

Bats actively prey on mosquitoes and other deleterious insects in rice paddies: Potential impact on human health and agriculture.

BACKGROUND: The fact that bats suppress agricultural pests has been measured for some particular dyads of predator and prey species in both economic and food security terms. The recent emergence of new molecular techniques allows for more precise screenings of bat's diet than the traditional visual identification systems and provides further evidence that bats consume an ample array of agricultural pest species. The main focus of the regulatory services that bats provide in agroecosystems has been on crop pests that cause yield losses. Rice paddies constitute a particular agronomic system with specific challenges, not only related to crop productivity but also to human health. Dipteran density in such ecosystems poses a serious threat to human wellbeing and hinders crop production. Mosquitoes cause direct harm to human populations, transmitting a number of infectious diseases. Non-biting midges (Chironomidae) can consume and weaken rice seedlings and can cause major yield losses. RESULTS: Mosquito populations and bat activity were assessed in rice paddies of Montgrí, Medes i Baix Ter Natural Park (NE Iberian Peninsula). Molecular analyses of bats faeces (6-weekly samples of 15 faeces each between mid-August and September) proved the presence of both mosquitoes and nonbiting midges in all diet samples. Furthermore, bat activity at the sampling locations was related to adult mosquito density. CONCLUSION: Our results suggest that bats actively exploit the emergence of adult mosquitoes and further prove that they prey on mosquitoes, nonbiting midges and other deleterious insects. Promoting the presence of bats next to human settlements in such agroecosystems may constitute a biological control system with direct impact on both human health and crop yield. © 2020 Society of Chemical Industry.

Second-growth and small forest clearings have little effect on the temporal activity patterns of Amazonian phyllostomid bats.

Secondary forests and human-made forest gaps are conspicuous features of tropical landscapes. Yet, behavioral responses to these aspects of anthropogenically modified forests remain poorly investigated. Here, we analyze the effects of small human-made clearings and secondary forests on tropical bats by examining the guild- and species-level activity patterns of phyllostomids sampled in the Central Amazon, Brazil. Specifically, we contrast the temporal activity patterns and degree of temporal overlap of 6 frugivorous and 4 gleaning animalivorous species in old-growth forest and second-growth forest and of 4 frugivores in old-growth forest and forest clearings. The activity patterns of frugivores and gleaning animalivores did not change between old-growth forest and second-growth, nor did the activity patterns of frugivores between old-growth forest and clearings. However, at the species level, we detected significant differences for Artibeus obscurus (old-growth forest vs. second-growth) and A. concolor (old-growth forest vs. clearings). The degree of temporal overlap was greater than random in all sampled habitats. However, for frugivorous species, the degree of temporal overlap was similar between old-growth forest and second-growth; whereas for gleaning animalivores, it was lower in second-growth than in old-growth forest. On the contrary, forest clearings were characterized by increased temporal overlap between frugivores. Changes in activity patterns and temporal overlap may result from differential foraging opportunities and dissimilar predation risks. Yet, our analyses suggest that activity patterns of bats in second-growth and small forest clearings, 2 of the most prominent habitats in humanized tropical landscapes, varies little from the activity patterns in old-growth forest.

Author Correction: A global database for metacommunity ecology, integrating species, traits, environment and space.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

A global database for metacommunity ecology, integrating species, traits, environment and space.

The use of functional information in the form of species traits plays an important role in explaining biodiversity patterns and responses to environmental changes. Although relationships between species composition, their traits, and the environment have been extensively studied on a case-by-case basis, results are variable, and it remains unclear how generalizable these relationships are across ecosystems, taxa and spatial scales. To address this gap, we collated 80 datasets from trait-based studies into a global database for metaCommunity Ecology: Species, Traits, Environment and Space; "CESTES". Each dataset includes four matrices: species community abundances or presences/absences across multiple sites, species trait information, environmental variables and spatial coordinates of the sampling sites. The CESTES database is a live database: it will be maintained and expanded in the future as new datasets become available. By its harmonized structure, and the diversity of ecosystem types, taxonomic groups, and spatial scales it covers, the CESTES database provides an important opportunity for synthetic trait-based research in community ecology.

Movement seasonality in a desert-dwelling bat revealed by miniature GPS loggers.

BACKGROUND: Bats are among the most successful desert mammals. Yet, our understanding of their spatio-temporal dynamics in habitat use associated with the seasonal oscillation of resources is still limited. In this study, we have employed state-of-the-art lightweight GPS loggers to track the yellow-winged bat Lavia frons in a desert in northern Kenya to investigate how seasonality in a desert affects the a) spatial and b) temporal dimensions of movements in a low-mobility bat. METHODS: Bats were tracked during April-May 2017 (rainy season) and January-February 2018 (dry season) using 1-g GPS loggers. Spatial and temporal dimensions of movements were quantified, respectively, as the home range and nightly activity patterns. We tested for differences between seasons to assess responses to seasonal drought. In addition, we quantified home range overlap between neighbouring individuals to investigate whether tracking data will be in accordance with previous reports on territoriality and social monogamy in L. frons. RESULTS: We obtained data for 22 bats, 13 during the rainy and 9 during the dry season. Home ranges averaged 5.46 ± 11.04 ha and bats travelled a minimum distance of 99.69 ± 123.42 m/hour. During the dry season, home ranges were larger than in the rainy season, and bats exhibited high activity during most of the night. No apparent association with free water was identified during the dry season. The observed spatial organisation of home ranges supports previous observations that L. frons partitions the space into territories throughout the year. CONCLUSIONS: Our results suggest that, in low-mobility bats, a potential way to cope with seasonally harsh conditions and resource scarcity in deserts is to cover larger areas and increase time active, suggesting lower cost-efficiency of the foraging activity. Climate change may pose additional pressures on L. frons and other low-mobility species by further reducing food abundances.

FragSAD: A database of diversity and species abundance distributions from habitat fragments.

Habitat destruction is the single greatest anthropogenic threat to biodiversity. Decades of research on this issue have led to the accumulation of hundreds of data sets comparing species assemblages in larger, intact, habitats to smaller, more fragmented, habitats. Despite this, little synthesis or consensus has been achieved, primarily because of non-standardized sampling methodology and analyses of notoriously scale-dependent response variables (i.e., species richness). To be able to compare and contrast the results of habitat fragmentation on species' assemblages, it is necessary to have the underlying data on species abundances and sampling intensity, so that standardization can be achieved. To accomplish this, we systematically searched the literature for studies where abundances of species in assemblages (of any taxa) were sampled from many habitat patches that varied in size. From these, we extracted data from several studies, and contacted authors of studies where appropriate data were collected but not published, giving us 117 studies that compared species assemblages among habitat fragments that varied in area. Less than one-half (41) of studies came from tropical forests of Central and South America, but there were many studies from temperate forests and grasslands from all continents except Antarctica. Fifty-four of the studies were on invertebrates (mostly insects), but there were several studies on plants (15), birds (16), mammals (19), and reptiles and amphibians (13). We also collected qualitative information on the length of time since fragmentation. With data on total and relative abundances (and identities) of species, sampling effort, and affiliated meta-data about the study sites, these data can be used to more definitively test hypotheses about the role of habitat fragmentation in altering patterns of biodiversity. There are no copyright restrictions. Please cite this data paper and the associated Dryad data set if the data are used in publications.

Secondary forest regeneration benefits old-growth specialist bats in a fragmented tropical landscape.

Tropical forest loss and fragmentation are due to increase in coming decades. Understanding how matrix dynamics, especially secondary forest regrowth, can lessen fragmentation impacts is key to understanding species persistence in modified landscapes. Here, we use a whole-ecosystem fragmentation experiment to investigate how bat assemblages are influenced by the regeneration of the secondary forest matrix. We surveyed bats in continuous forest, forest fragments and secondary forest matrix habitats, ~15 and ~30 years after forest clearance, to investigate temporal changes in the occupancy and abundance of old-growth specialist and habitat generalist species. The regeneration of the second growth matrix had overall positive effects on the occupancy and abundance of specialists across all sampled habitats. Conversely, effects on generalist species were negligible for forest fragments and negative for secondary forest. Our results show that the conservation potential of secondary forests for reverting faunal declines in fragmented tropical landscapes increases with secondary forest age and that old-growth specialists, which are often of most conservation concern, are the greatest beneficiaries of secondary forest maturation. Our findings emphasize that the transposition of patterns of biodiversity persistence in island ecosystems to fragmented terrestrial settings can be hampered by the dynamic nature of human-dominated landscapes.

Season-modulated responses of Neotropical bats to forest fragmentation.

Seasonality causes fluctuations in resource availability, affecting the presence and abundance of animal species. The impacts of these oscillations on wildlife populations can be exacerbated by habitat fragmentation. We assessed differences in bat species abundance between the wet and dry season in a fragmented landscape in the Central Amazon characterized by primary forest fragments embedded in a secondary forest matrix. We also evaluated whether the relative importance of local vegetation structure versus landscape characteristics (composition and configuration) in shaping bat abundance patterns varied between seasons. Our working hypotheses were that abundance responses are species as well as season specific, and that in the wet season, local vegetation structure is a stronger determinant of bat abundance than landscape-scale attributes. Generalized linear mixed-effects models in combination with hierarchical partitioning revealed that relationships between species abundances and local vegetation structure and landscape characteristics were both season specific and scale dependent. Overall, landscape characteristics were more important than local vegetation characteristics, suggesting that landscape structure is likely to play an even more important role in landscapes with higher fragment-matrix contrast. Responses varied between frugivores and animalivores. In the dry season, frugivores responded more to compositional metrics, whereas during the wet season, local and configurational metrics were more important. Animalivores showed similar patterns in both seasons, responding to the same group of metrics in both seasons. Differences in responses likely reflect seasonal differences in the phenology of flowering and fruiting between primary and secondary forests, which affected the foraging behavior and habitat use of bats. Management actions should encompass multiscale approaches to account for the idiosyncratic responses of species to seasonal variation in resource abundance and consequently to local and landscape scale attributes.