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.

Between roost contact is essential for maintenance of European bat lyssavirus type-2 in Myotis daubentonii bat reservoir: 'The Swarming Hypothesis'.

Many high-consequence human and animal pathogens persist in wildlife reservoirs. An understanding of the dynamics of these pathogens in their reservoir hosts is crucial to inform the risk of spill-over events, yet our understanding of these dynamics is frequently insufficient. Viral persistence in a wild bat population was investigated by combining empirical data and in-silico analyses to test hypotheses on mechanisms for viral persistence. A fatal zoonotic virus, European Bat lyssavirus type 2 (EBLV-2), in Daubenton's bats (Myotis daubentonii) was used as a model system. A total of 1839 M. daubentonii were sampled for evidence of virus exposure and excretion during a prospective nine year serial cross-sectional survey. Multivariable statistical models demonstrated age-related differences in seroprevalence, with significant variation in seropositivity over time and among roosts. An Approximate Bayesian Computation approach was used to model the infection dynamics incorporating the known host ecology. The results demonstrate that EBLV-2 is endemic in the study population, and suggest that mixing between roosts during seasonal swarming events is necessary to maintain EBLV-2 in the population. These findings contribute to understanding how bat viruses can persist despite low prevalence of infection, and why infection is constrained to certain bat species in multispecies roosts and ecosystems.

The movement ecology of the Mauritian flying fox (Pteropus niger): a long-term study using solar-powered GSM/GPS tags.

BACKGROUND: Flying foxes (Chiroptera: Pteropodidae) are large bats that often roost in the sun, hence solar-powered GPS/GSM devices can track their movements over extended periods. The endemic Mauritian flying fox (Pteropus niger) has recently been subjected to large-scale culling because of perceived damage to commercial fruit, and a consequent reduction in numbers of > 50% since 2015 resulted in its IUCN Red List Status being up-listed to Endangered. Determining its movements will be important for management and conservation, for understanding potential responses to environmental change, and for understanding population admixture. METHODS: Twelve bats were tagged with solar-powered GPS/GSM devices in 2014-2016. Tags remained active for up to almost a year (maximum 359 days: average 139 days (males) and 93 days (females)), providing some of the longest-term data on the movement ecology of bats yet obtained. Eight bats were probably hunted illegally, highlighting the scale of unauthorised persecution. RESULTS: Males travelled on average 9 km each night, females 6 km. The nightly distance covered by adults of both sexes was higher in winter than in summer, though the opposite pattern occurred for immature males. These differences are probably related to seasonal changes in fruit availability (adults) and to dispersal by immature males. The maximum distance covered during one night was > 92 km. Home ranges of males averaged 74,633 ha, females 31,072 ha. Core foraging areas averaged 2222 ha for males, 1364 ha for females. Fifty roosts were identified, mainly in forest fragments. As the bats disperse seeds of native plants that form forest canopies, conservation of the bats will potentially maintain and enhance native forest cover, in turn providing roosting sites for the bats. CONCLUSIONS: Solar-powered GSM tagging provides unprecedented potential for understanding the movement ecology of flying foxes. Mauritian flying foxes often move between the few remnant native forest fragments, which remain important for their conservation, and have potentially important roles in seed dispersal. Their nomadic movement fits with their panmictic genetic structure. Although their ability for long distance movements, sometimes over short timescales, permits rapid responses to local threats and environmental change, being restricted to Mauritius renders the bats extremely vulnerable to intense culling.

Flying foxes create extensive seed shadows and enhance germination success of pioneer plant species in deforested Madagascan landscapes.

Seed dispersal plays a significant role in forest regeneration and maintenance. Flying foxes are often posited as effective long-distance seed dispersers due to their large home ranges and ability to disperse seeds when flying. We evaluate the importance of the Madagascan flying fox Pteropus rufus in the maintenance and regeneration of forests in one of the world's priority conservation areas. We tested germination success of over 20,000 seeds from the figs Ficus polita, F. grevei and F. lutea extracted from bat faeces and ripe fruits under progressively more natural conditions, ranging from petri-dishes to outdoor environments. Seeds from all fig species showed increased germination success after passing through the bats' digestive tracts. Outside, germination success in F. polita was highest in faecal seeds grown under semi-shaded conditions, and seeds that passed through bats showed increased seedling establishment success. We used data from feeding trials and GPS tracking to construct seed shadow maps to visualize seed dispersal patterns. The models use Gaussian probability density functions to predict the likelihood of defecation events occurring after feeding. In captivity, bats had short gut retention times (often < 30 mins), but were sometimes able to retain seeds for over 24h. In the wild, bats travelled 3-5 km within 24-280 min after feeding, when defecation of ingested seeds is very likely. They produced extensive seed shadows (11 bats potentially dispersing seeds over 58,000 ha over 45 total days of tracking) when feeding on figs within their large foraging areas and dispersed the seeds in habitats that were often partially shaded and hence would facilitate germination up to 20 km from the feeding tree. Because figs are important pioneer species, P. rufus is an important dispersal vector that makes a vital contribution to the regeneration and maintenance of highly fragmented forest patches in Madagascar.

Habitat Preferences of Soprano Pipistrelle Pipistrellus pygmaeus (Leach, 1825) and Common Pipistrelle Pipistrellus pipistrellus (Schreber, 1774) in Two Different Woodlands in North East Scotland.

Alek Rachwald, Tim Bradford, Zbigniew Borowski, and Paul A. Racey (2016) The habitat preferences of the soprano pipistrelle Pipistrellus pygmaeus and the common pipistrelle Pipistrellus pipistrellus living in sympatry, were investigated in north east Scotland, using bat detector transects. Bat flight, foraging and social activity in natural birch woodland was compared with that in managed non-native coniferous woodland. Each area consists of riparian habitat, meadow-forest ecotone and dense forest. The activity of bats was highest in riparian habitat, then meadow, and lowest in dense woodland. P. pygmaeus was more abundant than P. pipistrellus in both areas, although in managed coniferous woodland only narrowly so (43.7% of all recorded bat flights, compared to 40.0% for common pipistrelle). In natural birch woodland, meadow habitat was most preferred by P. pipistrellus, and there was no significant difference between the use of riparian and woodland habitats, whereas in coniferous woodland, riparian habitat was most preferred. P. pygmaeus in both sites preferred riparian habitat, then meadow and forest least of all. The foraging activity of soprano pipistrelles was higher in birch than in coniferous woodland, whereas for the common pipistrelle, it was more evenly distributed. In both sites the lowest number of feeding buzzes was recorded in dense forest. In both study areas social calls were recorded, but many more for P. pygmaeus than for P. pipistrellus, especially in birch woodland. Soprano pipistrelle is a specialist species, focused mostly on riparian habitat, whereas common pipistrelle shows more generalistic behaviour. High number of social calls recorded near the waterbodies could suggest, that such habitat partitioning could be caused also by competitive behaviour.

Species undersampling in tropical bat surveys: effects on emerging biodiversity patterns.

Undersampling is commonplace in biodiversity surveys of species-rich tropical assemblages in which rare taxa abound, with possible repercussions for our ability to implement surveys and monitoring programmes in a cost-effective way. We investigated the consequences of information loss due to species undersampling (missing subsets of species from the full species pool) in tropical bat surveys for the emerging patterns of species richness (SR) and compositional variation across sites. For 27 bat assemblage data sets from across the tropics, we used correlations between original data sets and subsets with different numbers of species deleted either at random, or according to their rarity in the assemblage, to assess to what extent patterns in SR and composition in data subsets are congruent with those in the initial data set. We then examined to what degree high sample representativeness (r ≥ 0·8) was influenced by biogeographic region, sampling method, sampling effort or structural assemblage characteristics. For SR, correlations between random subsets and original data sets were strong (r ≥ 0·8) with moderate (ca. 20%) species loss. Bias associated with information loss was greater for species composition; on average ca. 90% of species in random subsets had to be retained to adequately capture among-site variation. For nonrandom subsets, removing only the rarest species (on average c. 10% of the full data set) yielded strong correlations (r > 0·95) for both SR and composition. Eliminating greater proportions of rare species resulted in weaker correlations and large variation in the magnitude of observed correlations among data sets. Species subsets that comprised ca. 85% of the original set can be considered reliable surrogates, capable of adequately revealing patterns of SR and temporal or spatial turnover in many tropical bat assemblages. Our analyses thus demonstrate the potential as well as limitations for reducing survey effort and streamlining sampling protocols, and consequently for increasing the cost-effectiveness in tropical bat surveys or monitoring programmes. The dependence of the performance of species subsets on structural assemblage characteristics (total assemblage abundance, proportion of rare species), however, underscores the importance of adaptive monitoring schemes and of establishing surrogate performance on a site by site basis based on pilot surveys.

White-nose syndrome: is this emerging disease a threat to European bats?

White-nose syndrome (WNS) is a newly emergent disease that potentially threatens all temperate bat species. A recently identified fungus, Geomyces destructans, is the most likely causative agent of this disease. Until 2009, WNS and G. destructans were exclusively known from North America, but recent studies have confirmed this fungus is also present in Europe. We assembled an international WNS consortium of 67 scientists from 29 countries and identified the most important research and conservation priorities to assess the risk of WNS to European bats. Here, we review what is known about WNS and G. destructans and detail the conservation and research recommendations aimed at understanding and containing this emerging infectious disease.

Positive selection of the bat interferon alpha gene family.

Type I interferons (IFNs) are produced by leukocytes in reaction to pathogenic infection and function as positive mediators in antiviral pathways. Among IFNs, IFN alpha (IFNA) has the largest number of family members and plays an important role against the invasion of pathogens. Bats are putative and proven vectors for numerous viruses; however, the evolution of the IFNA family in bats has not been addressed. Here, we construct a phylogeny of IFNA families, including one fruit bat (Dobsonia viridis), with other vertebrates as references. Site-model estimation reveals that positive selection has shaped bat IFNA genes, showing that positive selection drives the evolution of bat IFNA genes.

A comparative study of prenatal development in Miniopterus schreibersii fuliginosus, Hipposideros armiger and H. pratti.

BACKGROUND: Bats comprise the second largest order of mammals. However, there are far fewer morphological studies of post-implantation embryonic development than early embryonic development in bats. RESULTS: We studied three species of bats (Miniopterus schreibersii fuliginosus, Hipposideros armiger and H. pratti), representing the two suborders Yangochiroptera and Yinpterochiroptera. Using an established embryonic staging system, we identified the embryonic stages for M. schreibersii fuliginosus, H. armiger and H. pratti and described the morphological changes in each species, including the development of the complex and distinctive nose-leaves in H. armiger and H. pratti. Finally, we compared embryonic and fetal morphology of the three species in the present study with five other species for which information is available. CONCLUSION: As a whole, the organogenetic sequence of bat embryos is uniform and the embryos appear homoplastic before Stage 16. Morphological differentiation between species occurs mainly after embryonic Stage 16. Our study provides three new bat species for interspecific comparison of post-implantation embryonic development within the order Chiroptera and detailed data on the development of nose-leaves for bats in the superfamily Rhinolophoidea.

The aversive effect of electromagnetic radiation on foraging bats: a possible means of discouraging bats from approaching wind turbines.

Large numbers of bats are killed by collisions with wind turbines and there is at present no accepted method of reducing or preventing this mortality. Following our demonstration that bat activity is reduced in the vicinity of large air traffic control and weather radars, we tested the hypothesis that an electromagnetic signal from a small portable radar can act as a deterrent to foraging bats. From June to September 2007 bat activity was compared at 20 foraging sites in northeast Scotland during experimental trials (radar switched on) and control trials (no radar signal). Starting 45 minutes after sunset, bat activity was recorded for a period of 30 minutes during each trial and the order of trials were alternated between nights. From July to September 2008 aerial insects at 16 of these sites were sampled using two miniature light-suction traps. At each site one of the traps was exposed to a radar signal and the other functioned as a control. Bat activity and foraging effort per unit time were significantly reduced during experimental trials when the radar antenna was fixed to produce a unidirectional signal therefore maximising exposure of foraging bats to the radar beam. However, although bat activity was significantly reduced during such trials, the radar had no significant effect on the abundance of insects captured by the traps.

Molecular cloning and evolutionary analysis of hemoglobin alpha-chain genes in bats.

Bats are the only mammals with the capacity for powered flight. When flying, they need abundant energy and oxygen. According to previous works, the hemoglobin (Hb) oxygen loading function of bats is insensitive to variations in body temperature, although different bat species have different heat sensitivity. We cloned Hb alpha-chain sequences from eight bat species to investigate whether they have different characteristics. We found that Hb in the bat lineages is under purifying selection, which accords with the importance of its function in bats. Three turn regions in bat Hb, however, have distinct evolutionary rates compared with those of other mammals, and the codons in these regions have an accelerated rate of evolution. These codons are under divergent selection in bats. These changes in Hb may have occurred in response to the physiological requirements of the species concerned, as adaptations to different lifestyles.

Variations in the sequences of BMP2 imply different mechanisms for the evolution of morphological diversity in vertebrates.

Bone morphogenetic protein 2 (BMP2) plays an important role in skeletogenesis, osteoblastic differentiation and limb patterning. Its protein coding region consists of the signal peptide, the pro-domain (that regulates post-translational control of synthesis) and the mature domain (that carries out gene function). This gene has been considered previously to be conserved. By re-analyzing the coding region of BMP2 in 31 species of vertebrates, we found that the mature domain region is indeed conserved in mammals, but not among non-mammalian taxa. Moreover, compared to the mature domain, the signal peptide and pro-domain have experienced dramatic variation in all vertebrates. Six amino acid sites in the pro-domain were identified to be under diversifying Darwinian selection in mammals. These results indicate that the signal peptide and pro-domain of BMP2 may be involved in skeletal poly-morphology during mammal evolution and the mature domain may also contribute to this function in non-mammals. This supports the hypothesis that morphological variations in mammals result mainly from a change in post-translational control of synthesis, whereas in non-mammals they result mainly from gene functional change.

Spatial distribution of mitochondrial and microsatellite DNA variation in Daubenton's bat within Scotland.

Daubenton's bat (Myotis daubentonii) is a known reservoir for European bat lyssavirus type 2 (EBLV-2). An appreciation of the potential for epidemiological spread and disease risk requires an understanding of the dispersal of the primary host, and any large-scale geographical barriers that may impede gene flow. The spatial pattern of microsatellite and mitochondrial DNA variation was examined to infer patterns of dispersal of bats among 35 populations across Scotland. DNA sequence variation at the mitochondrial control region and ND1 genes revealed two distinct phylogeographical clades, with generally nonoverlapping geographical distributions except for a small number of populations where both matrilines were found in sympatry. Such discontinuity suggests that Scotland was recolonized twice following the retreat of the Pleistocene ice sheet with little subsequent matrilineal introgression. However, eight microsatellite loci showed low levels of genetic divergence among populations, even between populations from the two distinct mitochondrial DNA clades. An overall, macrogeographical genetic isolation-by-distance pattern was observed, with high levels of gene flow among local populations. Apparently contrasting patterns of mitochondrial and microsatellite divergence at different scales could be explained by sex-specific differences in gene flow at large scales.

Temporal changes in kin structure through a population cycle in a territorial bird, the red grouse Lagopus lagopus scoticus.

Populations of red grouse (Lagopus lagopus scoticus) undergo regular multiannual cycles in abundance. The 'kinship hypothesis' posits that such cycles are caused by changes in kin structure among territorial males producing delayed density-dependent changes in aggressiveness, which in turn influence recruitment and regulate density. The kinship hypothesis makes several specific predictions about the levels of kinship, aggressiveness and recruitment through a population cycle: (i) kin structure will build up during the increase phase of a cycle, but break down prior to peak density; (ii) kin structure influences aggressiveness, such that there will be a negative relationship between kinship and aggressiveness over the years; (iii) as aggressiveness regulates recruitment and density, there will be a negative relationship between aggressiveness in one year and both recruitment and density in the next; (iv) as kin structure influences recruitment via an affect on aggressiveness, there will be a positive relationship between kinship in one year and recruitment the next. Here we test these predictions through the course of an 8-year cycle in a natural population of red grouse in northeast Scotland, using microsatellite DNA markers to resolve changing patterns of kin structure, and supra-orbital comb height of grouse as an index of aggressiveness. Both kin structure and aggressiveness were dynamic through the course of the cycle, and changing patterns were entirely consistent with the expectations of the kinship hypothesis. Results are discussed in relation to potential drivers of population regulation and implications of dynamic kin structure for population genetics.

Bats avoid radar installations: could electromagnetic fields deter bats from colliding with wind turbines?

Large numbers of bats are killed by collisions with wind turbines, and there is at present no direct method of reducing or preventing this mortality. We therefore determine whether the electromagnetic radiation associated with radar installations can elicit an aversive behavioural response in foraging bats. Four civil air traffic control (ATC) radar stations, three military ATC radars and three weather radars were selected, each surrounded by heterogeneous habitat. Three sampling points matched for habitat type and structure, dominant vegetation species, altitude and surrounding land class were located at increasing distances from each station. A portable electromagnetic field meter measured the field strength of the radar at three distances from the source: in close proximity (<200 m) with a high electromagnetic field (EMF) strength >2 volts/metre, an intermediate point within line of sight of the radar (200-400 m) and with an EMF strength <2 v/m, and a control site out of sight of the radar (>400 m) and registering an EMF of zero v/m. At each radar station bat activity was recorded three times with three independent sampling points monitored on each occasion, resulting in a total of 90 samples, 30 of which were obtained within each field strength category. At these sampling points, bat activity was recorded using an automatic bat recording station, operated from sunset to sunrise. Bat activity was significantly reduced in habitats exposed to an EMF strength of greater than 2 v/m when compared to matched sites registering EMF levels of zero. The reduction in bat activity was not significantly different at lower levels of EMF strength within 400 m of the radar. We predict that the reduction in bat activity within habitats exposed to electromagnetic radiation may be a result of thermal induction and an increased risk of hyperthermia.