Patterns and causes of geographic variation in bat echolocation pulses

Evolutionary biologists have a long‐standing interest in how acoustic signals in animals vary geographically, because divergent ecology and sensory perception play an important role in speciation. Geographic comparisons are valuable in determining the factors that influence divergence of acoustic signals. Bats are social mammals and they depend mainly on echolocation pulses to locate prey, to navigate and to communicate. Mounting evidence shows that geographic variation of bat echolocation pulses is common, with a mean 5–10 kHz differences in peak frequency, and a high level of individual variation may be nested in this geographical variation. However, understanding the geographic variation of echolocation pulses in bats is very difficult, because of differences in sample and statistical analysis techniques as well as the variety of factors shaping the vocal geographic evolution. Geographic differences in echolocation pulses of bats generally lack latitudinal, longitudinal and elevational patterns, and little is known about vocal dialects. Evidence is accumulating to support the fact that geographic variation in echolocation pulses of bats may be caused by genetic drift, cultural drift, ecological selection, sexual selection and social selection. Future studies could relate geographic differences in echolocation pulses to social adaptation, vocal learning strategies and patterns of dispersal. In addition, new statistical techniques and acoustic playback experiments may help to illustrate the causes and consequences of the geographic evolution of echolocation pulse in bats.     

Bats adjust temporal parameters of echolocation pulses but not those of communication calls in response to traffic noise

Many studies based on acute short‐term noise exposure have demonstrated that animals can adjust their vocalizations in response to ambient noise. However, the effects of chronic noise over a relatively long time scale of multiple days remain largely unclear. Bats rely mainly on acoustic signals for perception of environmental and social communication. Nearly all previous studies on noise‐induced vocal adjustments have focused on echolocation pulse sounds. Relatively little is known regarding the effects of noise on social communication calls. Here, we examined the dynamic changes in the temporal parameters of echolocation and communication vocalizations of Vespertilio sinensis when exposed to traffic noise over multiple days. We found that the bats started to modify their echolocation vocalizations on the fourth day of noise exposure, with an increase of 42–91% in the total number of pulse sequences per day. Under noisy conditions, the number of pulses within a pulse sequence decreased by an average of 17.2%, resulting in a significantly slower number of pulses/sequence (P < 0.001). However, there was little change in the duration of a pulse sequence. These parameters were not significantly adjusted in most communication vocalizations under the noise condition (all P > 0.05), except that the duration decreased and the number of syllables/sequences increased in 1 type of communicative vocalization (P < 0.05). This study suggests that bats routinely adjust temporal parameters of echolocation but rarely of communication vocalizations in response to noise condition.     

Faeces as a novel material to estimate lyssavirus prevalence in bat populations

Rabies is caused by infection with a lyssavirus. Bat rabies is of concern for both public health and bat conservation. The current method for lyssavirus prevalence studies in bat populations is by oral swabbing, which is invasive for the bats, dangerous for handlers, time‐consuming and expensive. In many situations, such sampling is not feasible, and hence, our understanding of epidemiology of bat rabies is limited. Faeces are usually easy to collect from bat colonies without disturbing the bats and thus could be a practical and feasible material for lyssavirus prevalence studies. To further explore this idea, we performed virological analysis on faecal pellets and oral swabs of seven serotine bats (Eptesicus serotinus) that were positive for European bat 1 lyssavirus in the brain. We also performed immunohistochemical and virological analyses on digestive tract samples of these bats to determine potential sources of lyssavirus in the faeces. We found that lyssavirus detection by RT‐qPCR was nearly as sensitive in faecal pellets (6/7 bats positive, 86%) as in oral swabs (7/7 bats positive, 100%). The likely source of lyssavirus in the faeces was virus excreted into the oral cavity from the salivary glands (5/6 bats positive by immunohistochemistry and RT‐qPCR) or tongue (3/4 bats positive by immunohistochemistry) and swallowed with saliva. Virus could not be isolated from any of the seven faecal pellets, suggesting the lyssavirus detected in faeces is not infectious. Lyssavirus detection in the majority of faecal pellets of infected bats shows that this novel material should be further explored for lyssavirus prevalence studies in bats.     

Social and ecological complexity is associated with gestural repertoire size of wild chimpanzees

Increasing our understanding of primate gestural communication can provide new insights into language evolution. A key question in primate communication is the association between the social relationships of primates and their repertoire of gestures. Such analyses can reveal how primates use their repertoire of gestural communication to maintain their networks of family and friends, much as humans use language to maintain their social networks. In this study we examined the association between the repertoire of gestures (overall, manual and bodily gestures, and gestures of different modalities) and social bonds (presence of reciprocated grooming), coordinated behaviors (travel, resting, co‐feeding), and the complexity of ecology (e.g. noise, illumination) and sociality (party size, audience), in wild East African chimpanzees (Pan troglodytes schweinfurthii). A larger repertoire size of manual, visual gestures was associated with the presence of a relationship based on reciprocated grooming and increases in social complexity. A smaller repertoire of manual tactile gestures occurred when the relationship was based on reciprocated grooming. A smaller repertoire of bodily gestures occurred between partners who jointly traveled for longer. Whereas gesture repertoire size was associated with social complexity, complex ecology also influenced repertoire size. The evolution of a large repertoire of manual, visual gestures may have been a key factor that enabled larger social groups to emerge during evolution. Thus, the evolution of the larger brains in hominins may have co‐occurred with an increase in the cognitive complexity underpinning gestural communication and this, in turn, may have enabled hominins to live in more complex social groups.     

Knowledge,perceptions and attitude of a community living around a colony of straw‐coloured fruit bats (Eidolon helvum) in Ghana after Ebola virus disease outbreak in West Africa

A large population of straw‐coloured fruit bats (Eidolon helvum) colonizes a prime area in the city of Accra where several public amenities are located. Although the colony is positive to several zoonotic viruses including the Ebola virus, there is limited information on the social dimensions of the existence of the bats. As a step towards effective response to health risk and conservation of the bats, this study assessed the knowledge and attitude of the community living around the bats and determined their level of environmental and public health consciousness. The community generally lacks interest in bat bushmeat consumption but had low knowledge and disease risk perception of the bats. Despite major campaigns during the recent Ebola outbreak in West Africa, elements of risky behaviour including disbelief and disregard for some preventive measures and lack of interest in post‐bat exposure prophylaxis were recorded among a limited proportion of the community. There was the need to focus public health education on the community and possibly others that may have E. helvum colonies in West Africa.     

So much for the city: Urban–rural song variation in a widespread Asiatic songbird

Song plays a fundamental role in intraspecific communication in songbirds. The temporal and structural components of songs can vary in different habitats. These include urban habitats where anthropogenic sounds and alteration of habitat structure can significantly affect songbird vocal behavior. Urban–rural variations in song complexity, song length and syllable rate are not fully understood. In this study, using the oriental magpie‐robin (Copsychus saularis) as a model, we investigated urban–rural variation in song complexity, song length, syllable rate, syllable length and inter‐syllable interval. Comparing urban and rural songs from 7 countries across its natural Asiatic range (Bangladesh, India, Malaysia, Nepal, Singapore, Sri Lanka and Thailand), we found no significant differences in oriental magpie‐robin song complexity. However, we found significant differences in temporal song variables between urban and rural sites. Longer songs and inter‐syllable intervals in addition to slower syllable rates within urban sites contributed the most to this variance. This indicates that the urban environment may have driven production of longer and slower songs to maximize efficient transmission of important song information in urban habitats.     

Novel coronaviruses,astroviruses, adenoviruses and circoviruses in insectivorous bats from northern China

Bats are considered as the reservoirs of several emerging infectious disease, and novel viruses are continually found in bats all around the world. Studies conducted in southern China found that bats carried a variety of viruses. However, few studies have been conducted on bats in northern China, which harbours a diversity of endemic insectivorous bats. It is important to understand the prevalence and diversity of viruses circulating in bats in northern China. In this study, a total of 145 insectivorous bats representing six species were collected from northern China and screened with degenerate primers for viruses belonging to six families, including coronaviruses, astroviruses, hantaviruses, paramyxoviruses, adenoviruses and circoviruses. Our study found that four of the viruses screened for were positive and the overall detection rates for astroviruses, coronaviruses, adenoviruses and circoviruses in bats were 21.4%, 15.9%, 20% and 37.2%, respectively. In addition, we found that bats in northern China harboured a diversity of novel viruses. Common Serotine (Eptesicus serotinu), Fringed long‐footed Myotis (Myotis fimriatus) and Peking Myotis (Myotis pequinius) were investigated in China for the first time. Our study provided new information on the ecology and phylogeny of bat‐borne viruses.     

Extended‐spectrum beta‐lactamase‐producing Escherichia coli in common vampire bats Desmodus rotundus and livestock in Peru

Antibiotic resistance mediated by bacterial production of extended‐spectrum beta‐lactamase (ESBL) is a global threat to public health. ESBL resistance is most commonly hospital‐acquired; however, infections acquired outside of hospital settings have raised concerns over the role of livestock and wildlife in the zoonotic spread of ESBL‐producing bacteria. Only limited data are available on the circulation of ESBL‐producing bacteria in animals. Here, we report ESBL‐producing Escherichia coli in wild common vampire bats Desmodus rotundus and livestock near Lima, Peru. Molecular analyses revealed that most of this resistance resulted from the expression of bla_CTX‐M‐15 genes carried by plasmids, which are disseminating worldwide in hospital settings and have also been observed in healthy children of Peru. Multilocus sequence typing showed a diverse pool of E. coli strains carrying this resistance that were not always host species‐specific, suggesting sharing of strains between species or infection from a common source. This study shows widespread ESBL resistance in wild and domestic animals, supporting animal communities as a potential source of resistance. Future work is needed to elucidate the role of bats in the dissemination of antibiotic‐resistant strains of public health importance and to understand the origin of the observed resistance.     

Novel Borrelia genotypes in bats from the Macaregua Cave,Colombia

Bats have been implicated as reservoirs of relapsing fever group spirochaetes since the beginning of the last century. Recently, bat‐associated spirochaetes have been reported as human pathogens. In 1968, a spirochaete was detected in blood of the bat Natalus tumidirostris captured inside the Macaregua cave, Colombia. Data on this microorganism were never published again. The aim of this study was to evaluate the presence of Borrelia DNA in blood from bats of Macaregua cave. We performed molecular analyses using a genus‐specific real‐time PCR targeting the 16S rRNA to detect DNA of Borrelia in blood samples from 46 bats captured in the Macaregua cave. Positive samples were submitted to a battery of PCRs aiming to amply Borrelia 16S rRNA, flaB, glpQ, p66, ospC, clpA, clpX, nifS, pepX, pyrG, recG, rplB and uvrA genes. Seventeen samples were positive for Borrelia after real‐time PCR. With the exception of flaB gene, attempts to amplify further loci were unsuccessful. Nucleotide and amino acid divergences of four flaB haplotypes characterized from blood of Carollia perspicillata showed Borrelia burgdorferi sensu lato (Bbsl) as the most closely related group. A phylogenetic tree including 74 sequences of the genus confirmed this trend, since Borrelia genotypes detected in bats from Macaregua formed a monophyletic group basally positioned to Bbsl. Our results suggest that Borrelia genotypes characterized from bats roosting in the Macaregua cave might constitute a new taxon within the genus. This is the first molecular characterization of a Borrelia sp. in Colombia.     

No Evidence of Dengue Virus Infections in Several Species of Bats Captured in Central and Southern Mexico

Bats are reservoirs for viruses with zoonotic potential in the Americas, and scattered evidence exists suggesting that bats may act as reservoirs for dengue virus (DENV). To explore further the role of bats as part of DENV sylvatic cycles, 240 bats of 18 species were captured in 2 states of Mexico with contrasting ecological characteristics but concurrent DENV activity in humans. RT‐PCR analysis of RNA extracted from liver or spleen tissue from de bats failed to show evidence for the presence of DENV nucleic acids in these organs. In addition, plasma assayed by plaque reduction neutralization test showed no evidence of neutralizing anti‐DENV antibodies. These results suggest that American bats may not be reservoirs or amplification host for DENV infection.     

Toxoplasma gondii infection in Colombia with a review of hosts and their ecogeographic distribution

Toxoplasma gondii is one of the most prevalent zoonotic protozoan parasites among warm‐blooded animal populations (humans included) around the world, causing multiple clinic manifestations including death in the most severe cases of infection. Due to the versatile life cycle of T. gondii and its diversity of potential hosts, there is a common perception that natural areas and wildlife are highly prevalent reservoirs for the parasite; however, information and reports of the parasite on wildlife populations in Colombia are scarce. Using PRC‐based detection analyses of the B1 gene, we evaluated the presence of T. gondii in 49 native small mammal species (10% of the mammal species of Colombia) from 4 different undisturbed natural habitats. Additionally, to understand the ecogeographical distribution of the parasite in Colombia, we developed a literature search of infection reports including information on the host species, density of records and occurrence patterns (using landcover and ecoregions) in natural, rural and urban areas. Our literature review showed a total of 8,103 reports of T. gondii for Colombia of which 86% were related to humans, and 14% to non‐human mammals and other categories, with just a single report associated to wildlife; additionally, 82% of all reports were associated to urban areas whereas only 18% to rural sites. Based on the negative results for the presence of T. gondii in our PCR‐based analyses and our literature search, we suggest that T. gondii has a synanthropic distribution in Colombia occurring in ecoregions as variable as the xeric scrubs in the northern lowlands and humid montane Andean forests, also we show a lack of information on the parasite relationship with wildlife, a concerning fact given that zoonoses are the leading mechanism for the emergence of infectious diseases.     

When Ecological Information Meets High Wildlife Value Orientations: Influencing Preferences of Nearby Residents for Urban Wetlands

Preferences for landscapes are critical because they can drive landscape changes over time. The mediating role of wildlife value orientations in influencing preferences for urban wetlands through the provision of ecological information (based on insectivorous bats) was experimentally tested. Residents (N = 198) were asked about their preferences for wetlands, as depicted in 27 photographs. Half of the participants were provided with ecological information. Urban wetlands of high habitat quality for bats were preferred by both groups. There was a significant influence of ecological information on preference, although unexpectedly, this was on wetlands of low quality habitat; people who received ecological information had lower preferences for wetlands that provided lower quality habitat for bats. This influence was mediated by wildlife value orientations (wildlife rights and recreational wildlife experiences). Results suggest that preferences for landscapes can be influenced by providing information that is consistent with value orientations.     

Understanding Ebola virus and other zoonotic transmission risks through human–bat contacts: Exploratory study on knowledge,attitudes and practices in Southern Cameroon

The ecology of Ebola virus (EBV) remains largely unknown, but the previous detection of viral RNA and anti‐EBV antibodies in African bats suggests that they might play a role in the EBV reservoir. Moreover, African bats also carry other potentially zoonotic agents such as Henipah‐like viruses, coronaviruses and lyssaviruses. Today only little information is available on interactions between humans and bats. The objective of our exploratory study was to describe the extent and modes of contacts between humans and bats in southern Cameroon, considered as an area at risk for future EBV outbreaks. The survey was conducted in 11 villages of four distinct rural areas in southern Cameroon. A total of 135 respondents were interviewed using semi‐structured questionnaires, between February and May 2017. The study showed that direct contacts between bats and humans are relatively common. Bat bushmeat appeared to be an occasional meat resource; 40% of respondents consume bats with a median annual consumption of three, and 28% of respondents hunt them. About 22% of the respondents reported children catching bats. Indirect contact also appeared to be common; 55% of hunters use caves as shelters and 67% of interviewees eat fruits previously chewed by bats. Bat consumption varied significantly between regions (from 0% to 87%) and between pygmies and bantus in the extreme south‐east of Cameroon. The study revealed considerable diversity in practices among interviewees, most of them being subsistence cultivators and relying on self‐hunted bushmeat. Geographical diversity of contacts and perceptions regarding bats in Cameroon emphasizes the need to adjust zoonotic pathogen surveillance and education campaigns to the specificities of the communities and their context of interaction with wildlife.     

Serological evidence of widespread exposure of Grenada fruit bats to chikungunya virus

Antibody detection against selected potentially zoonotic vector‐borne alphaviruses and flaviviruses was conducted on sera from bats from all six parishes in Grenada, West Indies. Sera were tested for (i) antibodies to flaviviruses West Nile virus, St. Louis encephalitis virus, Ilhéus virus, Bussuquara virus (BSQV), Rio Bravo virus and all four serotypes of dengue virus (DENV) by plaque reduction neutralization test (PRNT); (ii) antibodies to alphaviruses western equine encephalitis virus, Venezuelan equine encephalitis virus and eastern equine encephalitis virus by epitope‐blocking enzyme‐linked immunosorbent assay (ELISA); and (iii) antibodies to the alphavirus chikungunya (CHIKV) by PRNT. Two species of fruit bats were sampled, Artibeus jamaicensis and Artibeus lituratus, all roosting in or within 1,000 m of human settlements. Fifteen (36%) of the 42 bats tested for neutralizing antibodies to CHIKV were positive. The CHIKV‐seropositive bats lived in localities spanning five of the six parishes. All 43 bats tested for epitope‐blocking ELISA antibody to the other alphaviruses were negative, except one positive for Venezuelan equine encephalitis virus. All 50 bats tested for neutralizing antibody to flaviviruses were negative, except one that had a BSQV PRNT₈₀ titre of 20. The CHIKV serology results indicate that bats living close to and within human settlements were exposed to CHIKV in multiple locations. Importantly, bats for this study were trapped a year after the introduction and peak of the human CHIKV epidemic in Grenada. Thus, our data indicate that bats were exposed to CHIKV possibly during a time of marked decline in human cases.     

Seed value influences cache pilfering rates by desert rodents

Some rodents gather and store seeds. How many seeds they gather and how they treat those seeds is largely determined by seed traits such as mass, nutrient content, hardness of the seed coat, presence of secondary compounds, and germination schedule. Through their consumption and dispersal of seeds, rodents act as agents of natural selection on seed traits, and those traits influence how rodents forage. Many seeds that are scatter‐hoarded by rodents are pilfered, or stolen, by other rodents, and seed traits also likely influence pilfering rates and seed fates of pilfered seeds. To clarify coevolutionary relationships between rodents and the plants that they disperse, one needs to understand the role of seed traits in rodent foraging decisions. We compared how the seeds of 4 species of plants that are dispersed by scatter‐hoarding animals and that differ in value (singleleaf piñon pine, Pinus monophylla; desert peach, Prunus andersonii; antelope bitterbrush, Purshia tridentata; Utah juniper, Juniperus osteosperma) were pilfered and recached by rodents. One hundred artificial caches of the 4 seed species (25 per species) were prepared, and removal by rodents was monitored. Rodents pilfered high‐value seeds more rapidly than the other seeds. Desert peach seeds, which contain toxic secondary compounds, were more frequently recached. Relatively low value seeds like Utah juniper and antelope bitterbrush were pilfered more slowly and were sometimes left at cache sites, and seeds of the latter species were transported shorter distances to new cache sites. The background density of seeds also appeared to influence the relative value of seeds.     

Avoiding bites and scratches? Understanding the public health implication of human–bat interactions in Ghana

Zoonotic pathogens cause an estimated 70% of emerging and re‐emerging infectious diseases in humans, affecting various aspects of human development on a global scale. The significance of bats as a source of emerging infectious diseases is being progressively appreciated. This study was undertaken post‐Ebola virus disease in West Africa and assessed the public health implications of human–bat interactions by exploring the reasons for contact between humans and bats, as well as reported actions taken upon experiencing bat bites or scratches. The paper highlights the nuances of human–bat interactions, stressing zoonotic disease risk awareness as well as the sources of information. The study used questionnaires to solicit information from 788 respondents in five communities with significant bat populations. We show that bat consumption was one of the main reasons for human–bat interactions. More men across the various communities ate bat meat. Only a small number of respondents (4.4%) reported being bitten by a bat, and 6.1% had been scratched by a bat. More than 21% had come into direct contact with bat blood. An even lower number went to the hospital after been bitten or scratched by bats. There was little knowledge on post‐exposure management. The most common places human–bat interactions occurred were at home and on farms. Seventy‐three per cent of the respondents believed that bats carried diseases, with Ebola virus disease being the most mentioned. Respondents indicated that the way they interacted with bats had not changed, even though they believed bats carried diseases and 46% stated that they had not changed the way they interacted with bats over the last two years. Apart from providing information on avoiding bites and scratches, a more holistic framework is needed to reduce human–bat interactions. The paper recommends a comprehensive and coordinated approach to optimizing an effective response to a potential bat‐borne zoonotic disease spillover.     

No Virological Evidence for an Influenza A ‐ like Virus in European Bats

New members of the influenza A virus genus have been detected recently in bats from South America. By molecular investigations, using a generic real‐time RT‐PCR (RT‐qPCR) that detects all previously known influenza A virus subtypes (H1‐H16) and a newly developed RT‐qPCR specific for the South American bat influenza‐like virus of subtype H17, a total of 1571 samples obtained from 1369 individual bats of 26 species from Central Europe were examined. No evidence for the occurrence of such influenza viruses was found. Further attempts towards a more comprehensive evaluation of the role of bats in the ecology and epidemiology of influenza viruses should be based on more intense monitoring efforts. However, given the protected status of bats, not only in Europe, such activities need to be embedded into existing pathogen‐monitoring programs.     

Detection of the Severe Acute Respiratory Syndrome‐Related Coronavirus and Alphacoronavirus in the Bat Population of Taiwan

Bats have been demonstrated to be natural reservoirs of severe acute respiratory syndrome coronavirus (SARS CoV) and Middle East respiratory syndrome (MERS) CoV. Faecal samples from 248 individuals of 20 bat species were tested for partial RNA‐dependent RNA polymerase gene of CoV and 57 faecal samples from eight bat species were tested positive. The highest detection rate of 44% for Scotophilus kuhlii, followed by 30% for Rhinolophus monoceros. Significantly higher detection rates of coronaviral RNA were found in female bats and Scotophilus kuhlii roosting in palm trees. Phylogenetic analysis classified the positive samples into SARS‐related (SARSr) CoV, Scotophilus bat CoV 512 close to those from China and Philippines, and Miniopterus bat CoV 1A‐related lineages. Coronaviral RNA was also detected in bat guano from Scotophilus kuhlii and Myotis formosus flavus on the ground and had potential risk for human exposure. Diverse bat CoV with zoonotic potential could be introduced by migratory bats and maintained in the endemic bat population in Taiwan.     

Bats as the main prey of wintering long‐eared owl (Asio otus) in Beijing: Integrating biodiversity protection and urban management

The loss of biodiversity from urbanized areas is a major environmental problem challenging policy‐makers throughout the world. Solutions to this problem are urgently required in China. We carried out a case study of wintering long‐eared owls (Asio otus) and their main prey to illustrate the negative effects of urbanization combined with ineffective conservation of biodiversity in Beijing. Field monitoring of owl numbers at two roosting sites from 2004 to 2012 showed that the owl population had fallen rapidly in metropolitan Beijing. Analysis of pellet contents identified only seven individuals of two species of shrew. The majority of mammalian prey comprised four bat and seven rodent species, making up 29.3% and 29.5% of the prey items, respectively. Prey composition varied significantly among years at the two sample sites. At the urban site the consumption of bats and rodents declined gradually over time, while predation on birds increased. In contrast, at the suburban site the prey composition showed an overall decrease in the number of bats, a sharp increase and a subsequent decrease in bird prey, and the number of rodent prey fell to a low point. Rapid development of real estate and inadequate greenfield management in city parks resulted in negative effects on the bird and small mammal habitat of urban areas in Beijing. We suggest that measures to conserve biodiversity should be integrated into future urban planning to maintain China's rich biodiversity while also achieving sustainable economic development.