Assessing roost disturbance of straw-coloured fruit bats (Eidolon helvum) through tri-axial acceleration.

The disturbance of wildlife by humans is a worldwide phenomenon that contributes to the loss of biodiversity. It can impact animals' behaviour and physiology, and this can lead to changes in species distribution and richness. Wildlife disturbance has mostly been assessed through direct observation. However, advances in bio-logging provide a new range of sensors that may allow measuring disturbance of animals with high precision and remotely, and reducing the effects of human observers. We used tri-axial accelerometers to identify daytime flights of roosting straw-coloured fruit bats (Eidolon helvum), which were used as a proxy for roost disturbance. This bat species roosts on trees in large numbers (often reaching hundreds of thousands of animals), making them highly vulnerable to disturbance. We captured and tagged 46 straw-coloured fruit bats with dataloggers, containing a global positioning system (GPS) and an accelerometer, in five roosts in Ghana, Burkina Faso and Zambia. Daytime roost flights were identified from accelerometer signatures and modelled against our activity in the roosts during the days of trapping, as a predictor of roost disturbance, and natural stressors (solar irradiance, precipitation and wind speed). We found that daytime roost flight probability increased during days of trapping and with increasing solar irradiance (which may reflect the search for shade to prevent overheating). Our results validate the use of accelerometers to measure roost disturbance of straw-coloured fruit bats and suggest that these devices may be very useful in conservation monitoring programs for large fruit bat species.

Foraging movements are density-independent among straw-coloured fruit bats.

Intraspecific competition in large aggregations of animals should generate density-dependent effects on foraging patterns. To test how large differences in colony size affect foraging movements, we tracked seasonal movements of the African straw-coloured fruit bat (Eidolon helvum) from four colonies that range from 4000 up to 10 million animals. Contrary to initial predictions, we found that mean distance flown per night (9-99 km), number of nightly foraging sites (2-3) and foraging and commuting times were largely independent of colony size. Bats showed classic central-place foraging and typically returned to the same day roost each night. However, roost switching was evident among individuals in three of the four colonies especially towards the onset of migration. The relatively consistent foraging patterns across seasons and colonies indicate that these bats seek out roosts close to highly productive landscapes. Once foraging effort starts to increase due to local resource depletion they migrate to landscapes with seasonally increasing resources. This minimizes high intraspecific competition and may help to explain why long-distance migration, otherwise rare in bats, evolved in this highly gregarious species.

Linking colony size with quantitative estimates of ecosystem services of African fruit bats.

Animal-mediated seed dispersal is a pivotal component of functioning forest ecosystems all over the globe. Animals that disperse seeds away from their parental plants increase the seeds' chances of survival by releasing them from competition and specialised predators and so contribute to maintain the biodiversity of forests. Furthermore, seeds dispersed into deforested areas provide the opportunity for reforestation. Forest regeneration especially depends on animals that cover large distances easily and cross forest gaps, in particular large-bodied frugivores or mobile species such as birds and bats [1]. Yet, frugivores have started to disappear from forests everywhere, with potentially dramatic consequences for forest composition, regeneration and overall forest biomass [2,3]. Identifying which species contribute substantially to the dispersal of viable seeds, and how these services are affected by fluctuations in population size, is thus pivotal to the understanding and conservation of forest ecosystems [4].

Highly diverse and antimicrobial susceptible Escherichia coli display a naïve bacterial population in fruit bats from the Republic of Congo.

Bats are suspected to be a reservoir of several bacterial and viral pathogens relevant to animal and human health, but studies on Escherichia coli in these animals are sparse. We investigated the presence of E. coli in tissue samples (liver, lung and intestines) collected from 50 fruit bats of five different species (Eidolon helvum, Epomops franqueti, Hypsignathus monstrosus, Myonycteris torquata, Rousettus aegyptiacus) of two different areas in the Republic of Congo between 2009 and 2010. To assess E. coli pathotypes and phylogenetic relationships, we determined the presence of 59 virulence associated genes and multilocus sequence types (STs). Isolates were further tested for their susceptibility to several antimicrobial substances by agar disk diffusion test and for the presence of an Extended-Spectrum Beta-Lactamase phenotype. E. coli was detected in 60% of the bats analysed. The diversity of E. coli strains was very high, with 37 different STs within 40 isolates. Occasionally, we detected sequence types (e.g. ST69, ST127, and ST131) and pathotypes (e.g. ExPEC, EPEC and atypical EPEC), which are known pathogens in human and/or animal infections. Although the majority of strains were assigned to phylogenetic group B2 (46.2%), which is linked with the ExPEC pathovar, occurrence of virulence-associated genes in these strains were unexpectedly low. Due to this, and as only few of the E. coli isolates showed intermediate resistance to certain antimicrobial substances, we assume a rather naïve E. coli population, lacking contact to humans or domestic animals. Future studies featuring in depth comparative whole genome sequence analyses will provide insights into the microevolution of this interesting strain collection.

Pronounced Seasonal Changes in the Movement Ecology of a Highly Gregarious Central-Place Forager, the African Straw-Coloured Fruit Bat (Eidolon helvum).

BACKGROUND: Straw-coloured fruit bats (Eidolon helvum) migrate over vast distances across the African continent, probably following seasonal bursts of resource availability. This causes enormous fluctuations in population size, which in turn may influence the bats' impact on local ecosystems. We studied the movement ecology of this central-place forager with state-of-the-art GPS/acceleration loggers and concurrently monitored the seasonal fluctuation of the colony in Accra, Ghana. Habitat use on the landscape scale was assessed with remote sensing data as well as ground-truthing of foraging areas. PRINCIPAL FINDINGS: During the wet season population low (~ 4000 individuals), bats foraged locally (3.5-36.7 km) in urban areas with low tree cover. Major food sources during this period were fruits of introduced trees. Foraging distances almost tripled (24.1-87.9 km) during the dry season population peak (~ 150,000 individuals), but this was not compensated for by reduced resting periods. Dry season foraging areas were random with regard to urban footprint and tree cover, and food consisted almost exclusively of nectar and pollen of native trees. CONCLUSIONS AND SIGNIFICANCE: Our study suggests that straw-coloured fruit bats disperse seeds in the range of hundreds of meters up to dozens of kilometres, and pollinate trees for up to 88 km. Straw-coloured fruit bats forage over much larger distances compared to most other Old World fruit bats, thus providing vital ecosystem services across extensive landscapes. We recommend increased efforts aimed at maintaining E. helvum populations throughout Africa since their keystone role in various ecosystems is likely to increase due to the escalating loss of other seed dispersers as well as continued urbanization and habitat fragmentation.

Investigating the zoonotic origin of the West African Ebola epidemic.

The severe Ebola virus disease epidemic occurring in West Africa stems from a single zoonotic transmission event to a 2-year-old boy in Meliandou, Guinea. We investigated the zoonotic origins of the epidemic using wildlife surveys, interviews, and molecular analyses of bat and environmental samples. We found no evidence for a concurrent outbreak in larger wildlife. Exposure to fruit bats is common in the region, but the index case may have been infected by playing in a hollow tree housing a colony of insectivorous free-tailed bats (Mops condylurus). Bats in this family have previously been discussed as potential sources for Ebola virus outbreaks, and experimental data have shown that this species can survive experimental infection. These analyses expand the range of possible Ebola virus sources to include insectivorous bats and reiterate the importance of broader sampling efforts for understanding Ebola virus ecology.

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.

Insecticide residues in bats along a land use-gradient dominated by cotton cultivation in northern Benin, West Africa.

Many regions in Africa are currently being converted from subsistence to cash crop farming such as cotton. Agricultural intensification is usually accompanied by increased use of pesticides, which can have an impact on non-target organisms. Bats are particularly sensitive to insecticide loads while providing substantial ecosystem services as predators of herbivorous insects. In this study, pesticide residues in bats in a landscape in northern Benin were investigated, which spanned a land use gradient from an agricultural zone dominated by cotton farms, through a buffer zone, and into a national park. Insecticides used in cotton cultivation, such as endosulfan, chlorpyrifos, flubendiamide, and spirotetramat, as well as persistent insecticides such as bis(4-chlorophenyl)-1,1,1-trichloroethane (DDT), lindane, and aldrine, were analysed. Insecticide residues detected in bats comprised DDT, endosulfan, and their corresponding transformation products. Maximum concentrations in the sampled bats were 11.2 mg/kg lipid of p,p'-DDE (median: 0.0136 mg/kg lipid) and 0.797 mg/kg lipid of ß-endosulfan (median: below detection limit [DL]). While insecticide concentrations were below lethal concentrations our data suggest that DDT had probably been recently used in the study region, and larger scale use would pose an increased risk for bat populations due to the high biomagnification of DDT.

Commuting fruit bats beneficially modulate their flight in relation to wind.

When animals move, their tracks may be strongly influenced by the motion of air or water, and this may affect the speed, energetics and prospects of the journey. Flying organisms, such as bats, may thus benefit from modifying their flight in response to the wind vector. Yet, practical difficulties have so far limited the understanding of this response for free-ranging bats. We tracked nine straw-coloured fruit bats (Eidolon helvum) that flew 42.5 ± 17.5 km (mean ± s.d.) to and from their roost near Accra, Ghana. Following detailed atmospheric simulations, we found that bats compensated for wind drift, as predicted under constant winds, and decreased their airspeed in response to tailwind assistance such that their groundspeed remained nearly constant. In addition, bats increased their airspeed with increasing crosswind speed. Overall, bats modulated their airspeed in relation to wind speed at different wind directions in a manner predicted by a two-dimensional optimal movement model. We conclude that sophisticated behavioural mechanisms to minimize the cost of transport under various wind conditions have evolved in bats. The bats' response to the wind is similar to that reported for migratory birds and insects, suggesting convergent evolution of flight behaviours in volant organisms.

High diversity of West African bat malaria parasites and a tight link with rodent Plasmodium taxa.

As the only volant mammals, bats are captivating for their high taxonomic diversity, for their vital roles in ecosystems--particularly as pollinators and insectivores--and, more recently, for their important roles in the maintenance and transmission of zoonotic viral diseases. Genome sequences have identified evidence for a striking expansion of and positive selection in gene families associated with immunity. Bats have also been known to be hosts of malaria parasites for over a century, and as hosts, they possess perhaps the most phylogenetically diverse set of hemosporidian genera and species. To provide a molecular framework for the study of these parasites, we surveyed bats in three remote areas of the Upper Guinean forest ecosystem. We detected four distinct genera of hemosporidian parasites: Plasmodium, Polychromophilus, Nycteria, and Hepatocystis. Intriguingly, the two species of Plasmodium in bats fall within the clade of rodent malaria parasites, indicative of multiple host switches across mammalian orders. We show that Nycteria species form a very distinct phylogenetic group and that Hepatocystis parasites display an unusually high diversity and prevalence in epauletted fruit bats. The diversity and high prevalence of novel lineages of chiropteran hemosporidians underscore the exceptional position of bats among all other mammalian hosts of hemosporidian parasites and support hypotheses of pathogen tolerance consistent with the exceptional immunology of bats.

A framework for the study of zoonotic disease emergence and its drivers: spillover of bat pathogens as a case study.

Many serious emerging zoonotic infections have recently arisen from bats, including Ebola, Marburg, SARS-coronavirus, Hendra, Nipah, and a number of rabies and rabies-related viruses, consistent with the overall observation that wildlife are an important source of emerging zoonoses for the human population. Mechanisms underlying the recognized association between ecosystem health and human health remain poorly understood and responding appropriately to the ecological, social and economic conditions that facilitate disease emergence and transmission represents a substantial societal challenge. In the context of disease emergence from wildlife, wildlife and habitat should be conserved, which in turn will preserve vital ecosystem structure and function, which has broader implications for human wellbeing and environmental sustainability, while simultaneously minimizing the spillover of pathogens from wild animals into human beings. In this review, we propose a novel framework for the holistic and interdisciplinary investigation of zoonotic disease emergence and its drivers, using the spillover of bat pathogens as a case study. This study has been developed to gain a detailed interdisciplinary understanding, and it combines cutting-edge perspectives from both natural and social sciences, linked to policy impacts on public health, land use and conservation.