The Iwokrama Rain Forest Programme for sustainable development: how much of Guyana's bat (Chiroptera) diversity does it encompass?

In 1989 Guyana designated 3600 km² of tropical rain forest as the Iwokrama Rain Forest Programme (IRFP) for developing methods of sustainable forest utilization and for conserving biodiversity. Bat diversity was assessed in 5 km² of the IRFP area over a ten-week period. Effort totalled 22 400 m² mist-net hours during 26 nights, 227 m² harp-trap hours during 8 nights and 28 person days searching for roosts. This revealed 38 species of bats. In comparison with two other neotropical sites alpha diversity was high as shown by a Shannon diversity index of 1.30 for the 33 species taken in foraging areas by mist net and harp trap.Four forest types found here show some of the lowest floristic diversity in the neotropics. The high motility of bats allows them to exploit the range of forest types available locally, so avoiding constraints imposed within any one forest type.A list of bat species known from Guyana was compiled from the literature. A total of 96 species were found plus 17 unsupported records. The list is presented together with a further 45 species that potentially could occur. Our survey has shown that 45 of the 96 species recorded in Guyana (47%) are known from the IRFP area, suggesting that it provides a good representation of Guyana's bat fauna.The work formed part of a Guyana Rain Forest biodiversity programme coordinated by Mike Gillman at The Open University, Walton Hall, Milton Keynes, MK7 6AA, England, UK.     

Comparative hindlimb bone morphology in noctilionid fisher bats (Chiroptera: Noctilionidae), with emphasis on Noctilio leporinus postnatal development

The hindlimbs allow bats to attach to the mother from birth, and roost during independent life. Despite the great morphological diversity in Chiroptera, the hindlimbs morphology and its postnatal development have been poorly studied. Postnatal development of hindlimbs in Noctilio leporinus is described, further comparing the morphology of adults with that of Noctilio albiventris and previously reported species (Desmodus rotundus, Artibeus lituratus, Molossus molossus). The ossification ending sequence at autopodium elements of N. leporinus does not follow the distal to proximal directional sequence described for D. rotundus, exhibiting a heterochronic delayed ossification ending for the digits of N. leporinus regarding other hindlimb elements, associated with the bigger relative autopodium size of this fisher bat regarding other bat species. Noctilionid bats share the same adult hindlimb bone morphology, except for differences at hindlimb proportions and calcar ossification degree. There are differences in the number and position of bony processes, slots and sesamoids of adult noctilionid fisher bats regarding previously reported species; most differences are concentrated at the autopodium and are related to an increased surface for muscular insertion and the structural support of claws. These facts seem to be closely associated with functional demands of the feeding strategy of noctilionid fisher bats.     

A bat (Chiroptera) survey of Mora rainforest in Trinidad's Victoria-Mayaro Forest Reserve

The bat fauna of the Mora excelsa-dominated rainforest in the Victoria-Mayaro Forest Reserve (VMFR) in south-east Trinidad was assessed over a six-week period. Trapping effort totaled 271 mist net hours and caught 143 bats of 22 species at a rate of one bat every two net-hours. Simpsons diversity index (1/D) was 1.28 for primary Mora forest and extrapolation using Chaos' estimator, a non-parametric method, estimated the total number of species as 39. Phyllostomid bats of the subfamilies Phyllostominae and Stenodermatinae were well represented, and frugivores predominated in number, accounting for 77% of all captures in primary forest. The most abundant bat, the ground-storey frugivore, Carollia perspicillata, accounted for 43% of all captures in primary forest and, in contrast to most bats, was also abundant on man-made paths through the forest. Four species not previously recorded from the reserve, Tonatia bidens, Trachops cirrhosus, a Myotis sp., and the rare Phylloderma stenops, were captured, bringing the total number of bats species known from the reserve to 35. Thus, over half (52%) of Trinidad's 67 bat species occur in this one forest reserve, making it a high priority area for effective protection and management.     

Characterization of fungi associated with the nasal hairs of Molossid bats

Fungal pathogens have become a serious threat to wildlife, threatening populations of even once common, abundant species. We describe the mycobiota associated with the nasal hairs of three Molossid bat species, Cynomops planirostris, Molossus molossus, and Molossus rufus, in southwest Brazil. Bats were captured in the Cerrado and Pantanal biomes. We cultured 22 fungal isolates from twelve individual bats. Sixteen sequences of the ITS region were obtained, yielding 11 unique sequence types from the genera Aspergillus, Cladosporium, Paecilomyces, and Penicillium. No obvious detrimental effects on the bats from the fungi were observed, although some species or genera that we identified are known pathogens in other species. This is the first report of such fungi associated with the nasal hairs of Molossid bats. Our results indicate the need for further research on the biodiversity, ecological role, and potential effects of this mycobiota on Molossid bats.     

Long-term bat study on an island in the southeastern Brazilian coast with comparison of richness and composition of species among sites

Although Rio de Janeiro is one of the best sampled states of Brazil for bats, there are still some poorly studied islands on its coast. Hence, we inventoried the bat species of an island on the southwestern coast of Rio de Janeiro, compared five sites sampled within this island, and compared its bat community with seven other sites in the same region. We carried out sampling in July 1995 and from September 2006 to August 2010, comprising 58 samplings. We captured a total of 1502 individuals of 25 bat species with mist nets set far from roosts, or close to or inside roosts. The most abundant species were Artibeus lituratus, Molossus molossus, and Carollia perspicillata. Total sampling effort was 89,400 m² h. The present study was one out of five inventories carried out in the southwestern coast of Rio de Janeiro that registered more than 1000 bat individuals from more than 24 bat species. Long-term inventories on islands are still needed, because they can result in a large number of species and captures as observed in the present study.     

Laboulbeniales hyperparasites (Fungi,Ascomycota) of bat flies: Independent origins and host associations

The aim of this study was to explore the diversity of ectoparasitic fungi (Ascomycota, Laboulbeniales) that use bat flies (Diptera, Hippoboscoidea) as hosts. Bat flies themselves live as ectoparasites on the fur and wing membranes of bats (Mammalia, Chiroptera); hence this is a tripartite parasite system. Here, we collected bats, bat flies, and Laboulbeniales, and conducted phylogenetic analyses of Laboulbeniales to contrast morphology with ribosomal sequence data. Parasitism of bat flies by Laboulbeniales arose at least three times independently, once in the Eastern Hemisphere (Arthrorhynchus) and twice in the Western Hemisphere (Gloeandromyces, Nycteromyces). We hypothesize that the genera Arthrorhynchus and Nycteromyces evolved independently from lineages of ectoparasites of true bugs (Hemiptera). We assessed phylogenetic diversity of the genus Gloeandromyces by considering the LSU rDNA region. Phenotypic plasticity and position‐induced morphological adaptations go hand in hand. Different morphotypes belong to the same phylogenetic species. Two species, G. pageanus and G. streblae, show divergence by host utilization. In our assessment of coevolution, we only observe congruence between the Old World clades of bat flies and Laboulbeniales. The other associations are the result of the roosting ecology of the bat hosts. This study has considerably increased our knowledge about bats and their associated ectoparasites and shown the necessity of including molecular data in Laboulbeniales taxonomy.     

Bat species diversity and distribution in a disturbed regime at the Lake Bogoria National Reserve,Kenya

Human population growth drives intrusion and progressive conversion of natural habitats for agriculture. We evaluated human impacts on bat species diversity and distribution among four vegetation types in and around Lake Bogoria National Reserve between November 2012 and July 2013. Plants were surveyed using the Braun–Blanquet cover/abundance method, whereas bats were sampled using standard mist nets erected on poles at ground level. Floristic similarity analysis revealed three broad vegetation assemblages, namely riverine vegetation, farmland and Acacia woodland/Acacia–Commiphora woodland. Two hundred and 33 bats representing eleven species in eleven genera and seven families were recorded. These were Epomophorus minimus, Rhinolophus landeri, Hipposideros caffer, Cardioderma cor, Lavia frons, Nycteris hispida, Chaerephon pumilus, Mops condylurus, Neoromicia capensis, Scotoecus hirundo and Scotophilus dinganii. Species richness estimators indicated that sampling for bats at ground level was exhaustive. Bat species richness and diversity were highest in the more structurally complex Acacia woodland compared to more homogenous farmlands where we recorded only common and generalist species that often occur in open habitats. The higher bat species richness and diversity in the Acacia woodland as compared to farmland underscore the importance of remnant natural savannah woodlands in the conservation of bats and other elements of biodiversity .     

DNA barcoding of Neotropical bats: species identification and discovery within Guyana

Sequence diversity in the cytochrome c oxidase subunit 1 gene has been shown to be an effective tool for species identification and discovery in various groups of animals, but has not been extensively tested in mammals. We address this gap by examining the performance of DNA barcodes in the discrimination of 87 species of bats from Guyana. Eighty‐one of these species showed both low intraspecific variation (mean = 0.60%), and clear sequence divergence from their congeners (mean = 7.80%), while the other six showed deeply divergent intraspecific lineages suggesting that they represent species complexes. Although further work is needed to examine patterns of sequence diversity at a broader geographical scale, the present study validates the effectiveness of barcoding for the identification of regional bat assemblages, even highly diverse tropical faunas.     

A Preliminary Study of Viral Metagenomics of French Bat Species in Contact with Humans: Identification of New Mammalian Viruses

The prediction of viral zoonosis epidemics has become a major public health issue. A profound understanding of the viral population in key animal species acting as reservoirs represents an important step towards this goal. Bats harbor diverse viruses, some of which are of particular interest because they cause severe human diseases. However, little is known about the diversity of the global population of viruses found in bats (virome). We determined the viral diversity of five different French insectivorous bat species (nine specimens in total) in close contact with humans. Sequence-independent amplification, high-throughput sequencing with Illumina technology and a dedicated bioinformatics analysis pipeline were used on pooled tissues (brain, liver and lungs). Comparisons of the sequences of contigs and unassembled reads provided a global taxonomic distribution of virus-related sequences for each sample, highlighting differences both within and between bat species. Many viral families were present in these viromes, including viruses known to infect bacteria, plants/fungi, insects or vertebrates, the most relevant being those infecting mammals (Retroviridae, Herpesviridae, Bunyaviridae, Poxviridae, Flaviviridae, Reoviridae, Bornaviridae, Picobirnaviridae). In particular, we detected several new mammalian viruses, including rotaviruses, gammaretroviruses, bornaviruses and bunyaviruses with the identification of the first bat nairovirus. These observations demonstrate that bats naturally harbor viruses from many different families, most of which infect mammals. They may therefore constitute a major reservoir of viral diversity that should be analyzed carefully, to determine the role played by bats in the spread of zoonotic viral infections.     

Assessing road effects on bats: the role of landscape, road features, and bat activity on road-kills

Recent studies suggest that roads can significantly impact bat populations. Though bats are one of the most threatened groups of European vertebrates, studies aiming to quantify bat mortality and determine the main factors driving it remain scarce. Between March 16 and October 31 of 2009, we surveyed road-killed bats daily along a 51-km-long transect that incorporates different types of roads in southern Portugal. We found 154 road-killed bats of 11 species. The two most common species in the study area, Pipistrellus kuhlii and P. pygmaeus, were also the most commonly identified road-kill, representing 72 % of the total specimens collected. About two-thirds of the total mortality occurred between mid July and late September, peaking in the second half of August. We also recorded casualties of threatened and rare species, including Miniopterus schreibersii, Rhinolophus ferrumequinum, R. hipposideros, Barbastella barbastellus, and Nyctalus leisleri. These species were found mostly in early autumn, corresponding to the mating and swarming periods. Landscape features were the most important variable subset for explaining bat casualties. Road stretches crossing or in the vicinity of high-quality habitats for bats—including dense Mediterranean woodland (“montado”) areas, water courses with riparian gallery, and water reservoirs—yielded a significantly higher number of casualties. Additionally, more road-killed bats were recorded on high-traffic road stretches with viaducts, in areas of higher bat activity and near known roosts.     

Knowledge and Perceptions of,and Attitudes to,Bats by People Living around Arabuko-Sokoke Forest,Malindi-Kenya

Bat populations continue to decline worldwide because of myriad human activities. To enhance bat conservation, human behavior needs to change. Such change can occur, in part, through an understanding of what motivates human actions toward bats. We used a Bat Attitude Questionnaire (BAQ) to investigate attitudes toward bats in people (n = 394) living around Arabuko-Sokoke Forest (ASF), Kenya. Belief in myths seemed to prevail among those surveyed and that these myths were significantly associated with low tolerance of bats (ordinal regression, p < 0.05). Older and more educated people reported more positive attitudes toward bats than others. Multiple linear regression revealed that females showed more negative attitudes toward, and more belief in, myths about bats than males (both p < 0.01). Ordinal regression showed that hostile behavior toward bats was more common among males (p < 0.001). Nearly one-third of the respondents reported actively killing bats or destroying bat roosts. A similar proportion did not see any benefits of bats to humans, while the majority of respondents associated bats with the destruction of farmers’ fruits. To address prevailing negative attitudes about bats, we recommend conducting evening school-based bat study tours, specifically targeting youths in schools around the forest, to examine whether physical contacts with bats would help positively influence human attitudes toward bats. Additionally, since mango (Mangifera indica) farming is an important source of income to people around ASF, an assessment of the quantity of mangoes destroyed by bats would be important to determine whether there is a need for controlling bat access to crops through appropriate schemes.     

Shade cacao plantations (<Emphasis Type="Italic">Theobroma cacao</Emphasis>) and bat conservation in southern Bahia,Brazil

Nearly 40% of the remaining Atlantic Forest in southern Bahia state, Brazil, is a rustic agroforest of cacao (Theobroma cacao). These traditional shade plantations, locally known as ‘cabrucas’, are habitats for forest dwelling species. Here we investigated the potential role of this traditional crop as a support for bat assemblages in southern Bahia, establishing the extent to which the bat community structure found in this agricultural system is influenced by the proximity of forest tracts. We compared the bat community attributes (richness, diversity and dominance) and species-level response (capture frequency) between native forest tracts and shade cacao plantations located in two distinct landscapes, which varied in total amount of forest (patch sizes and total forested area) and in their proximity to forest tracts. The cabrucas contiguous to forest tracts showed a rich and abundant bat community, with samples showing capture rates, species richness, diversity and evenness significantly higher than those reported for forest tracts. This situation changes, however, when shade plantations are located at some distance from forest tracts ( > 1000 m). Bat communities in these isolated cabrucas are less diverse than those found in forests and nearby cabrucas, but in both cases, species usually associated with pristine habitats were found. These findings suggest that cabrucas per se are not forest surrogates, and their potential to harbor forest dwelling bat species is closely linked with the existence of nearby forest tracts that may act as a source for species populations. Therefore, the entire landscape should be considered for management, taking into account that maintenance of cabrucas together with the preservation and restoration of forest patches is probably direly needed if one wishes to conserve the bat diversity in southern Bahia for the long term.     

Diversity of Bartonella and Rickettsia spp. in Bats and Their Blood-Feeding Ectoparasites from South Africa and Swaziland

In addition to several emerging viruses, bats have been reported to host multiple bacteria but their zoonotic threats remain poorly understood, especially in Africa where the diversity of bats is important. Here, we investigated the presence and diversity of Bartonella and Rickettsia spp. in bats and their ectoparasites (Diptera and Siphonaptera) collected across South Africa and Swaziland. We collected 384 blood samples and 14 ectoparasites across 29 different bat species and found positive samples in four insectivorous and two frugivorous bat species, as well as their Nycteribiidae flies. Phylogenetic analyses revealed diverse Bartonella genotypes and one main group of Rickettsia, distinct from those previously reported in bats and their ectoparasites, and for some closely related to human pathogens. Our results suggest a differential pattern of host specificity depending on bat species. Bartonella spp. identified in bat flies and blood were identical supporting that bat flies may serve as vectors. Our results represent the first report of bat-borne Bartonella and Rickettsia spp. in these countries and highlight the potential role of bats as reservoirs of human bacterial pathogens.     

Island biogeography of bats in Baja California, Mexico: patterns of bat species richness in a near-shore archipelago

Aim We studied the relationship between the size and isolation of islands and bat species richness in a near‐shore archipelago to determine whether communities of vagile mammals conform to predictions of island biogeography theory. We compared patterns of species richness in two subarchipelagos to determine whether area per se or differences in habitat diversity explain variations in bat species richness. Location Islands in the Gulf of California and adjacent coastal habitats on the Baja California peninsula in northwest Mexico. Methods Presence–absence surveys for bats were conducted on 32 islands in the Gulf of California using acoustic and mist‐net surveys. We sampled for bats in coastal habitats of four regions of the Baja peninsula to characterize the source pool of potential colonizing species. We fitted a semi‐log model of species richness and multiple linear regression and used Akaike information criterion model selection to assess the possible influence of log₁₀ area, isolation, and island group (two subarchipelagos) on the species richness of bats. We compared the species richness of bats on islands with greater vegetation densities in the southern gulf (n = 20) with that on drier islands with less vegetation in the northern gulf (n = 12) to investigate the relationship between habitat diversity and the species richness of bats. Results Twelve species of bats were detected on islands in the Gulf of California, and 15 species were detected in coastal habitats on the Baja peninsula. Bat species richness was related to both area and isolation of islands, and was higher in the southern subarchipelago, which has denser vegetation. Log₁₀ area was positively related to bat species richness, which increased by one species for every 5.4‐fold increase in island area. On average, richness declined by one species per 6.25 km increase in isolation from the Baja peninsula. Main conclusions Our results demonstrate that patterns of bat species richness in a near‐shore archipelago are consistent with patterns predicted by the equilibrium theory of island biogeography. Despite their vagility, bats may be more sensitive to moderate levels of isolation than previously expected in near‐shore archipelagos. Differences in vegetation and habitat xericity appear to be associated with richness of bat communities in this desert ecosystem. Although observed patterns of species richness were consistent with those predicted by the equilibrium theory, similar relationships between species richness and size and isolation of islands may arise from patch‐use decision making by individuals (optimal foraging strategies).     

Bats of Lithuania: distribution, status and protection

The Lithuanian bat fauna includes 14 species. Myotis daubentoni, Pipistrellus nathusii, Plecotus auritus and Eptesicus serotinus are the most abundant and widespread species, although recently P. auritus has disappeared from some hibernacula. There are still abundant populations of Myotis nattereri, Myotis brandti and Barbastella barbastellus in hibernacula, while their status in summer is unknown. Myotis dasycneme is probably very rare and endangered. The status of Myotis mystacinus and Nyctalus leisleri is not clear, but they are most likely very rare because very few specimens have been found. So far little is known about status of Nyctalus noctula, Pipistrellus pipistrellus, Eptesicus nilssoni and Vespertilio murinus because these species are common only during autumn bat migration along the Baltic Sea coast. Two other species, Myotis bechsteini and Rhinolophus hipposideros, have been rejected from the list of bats of Lithuania, because old references to records of these species were not reliable. From what is currently known it seems that: (i) the northern limits of distribution of B. barbastellus and E. serotinus reach the middle of Lithuania between 55°N and 56°N, which may also be the southern limit of abundance of E. nilssoni; (ii) the wintering site with the largest numbers of bats in Lithuania is the vaults of Kaunas fortress, where every year eight species are found hibernating in numbers estimated as follows: M. daubentoni 400–500, M. nattereri 200–300, M. brandti 80–100, B.barbastellus 200–300, P. auritus 40–60, M. dasycneme 15–20 and a few E. serotinus and E. nilssoni. In Lithuania nine bat species have been protected by law since 1991, as species included in the Red Data Book. Also 11 bat reserves have been designated in Kaunas fortress to protect the most important hibernation sites in Lithuania.     

No fever and leucocytosis in response to a lipopolysaccharide challenge in an insectivorous bat

Bat immune systems may allow them to respond to zoonotic agents more efficiently than other mammals. As the first line of defence, the taxonomically conserved acute phase immune reaction of leucocytosis and fever is crucial for coping with infections, but it is unknown if this response is a key constituent to bat immunological success. We investigated the acute phase reaction to a standard lipopolysaccharide (LPS) challenge in Pallas''s mastiff bats (Molossus molossus). Challenged bats lost mass, but in contrast to other mammals showed no leucocytosis or fever. There also was no influence on body temperature reduction during torpor. When compared to recent genome-wide assays for constituent immune genes, this lack of a conserved fever response to LPS contributes to a clearer understanding of the innate immune system in bat species and of the coevolution of bats with a wide diversity of pathogens.     

Diversity and host preference of leaf endophytic fungi in the Iwokrama Forest Reserve, Guyana

Endophytic fungi were isolated from living symptomless leaves of 12 tree species from two locations in the Iwokrama Forest Reserve, Guyana. Sixty-four fungal morphotaxa were characterized from 2492 cultures, which were derived from a total of 2520 sample units. Species of Colletotrichum, Nodulisporium, Pestalotiopsis and Phomopsis were most frequently isolated. Colonization was greater in samples from the midrib than in those from laminar tissue, and slightly greater at the tip of the lamina compared with the base of the leaf. In contrast to studies in temperate ecosystems, no distinct fungal communities were identified for individual plant species, suggesting that the degree of host preference is low. The implications for estimation of fungal diversity in tropical systems are explored.     

Community of bat flies (Streblidae and Nycteribiidae) on bats in the Cerrado of Central-West Brazil: hosts,aggregation, prevalence,infestation intensity,and infracommunities

Streblidae and Nycteribiidae are families of bloodsucking flies that parasitize bats exclusively. We studied the community of these flies in a Cerrado area in the Central-West Brazil. We captured 708 bats over 17 nights from October 2012 to March 2013. Forty-five per cent of the hosts were parasitized by 836 specimens of bat flies of 22 species. The most abundant flies were Trichobius joblingi on Carollia perspicillata, followed by Megistopoda aranea on Artibeus planirostris, and Strebla guajiro on C. perspicillata. All bat flies showed a high level of specificity for their hosts. Trichobius joblingi was the bat fly with the highest prevalence (80%) and mean intensity of infestation (3.5) on hosts with a representative sample size (n > 20). This result is likely related to the type of roosting (cavity) used by C. perspicillata, primary host of this fly species. Anoura caudifer hosted the largest infracommunities (n = 7). However, most bats were parasitized by a single fly species, suggesting a pattern in infestations. The aggregation index was high, indicating an unequal occurrence in parasite infestations. The majority of hosts were infested by few or no flies and few hosts were highly infested, showing a negative binomial distribution.     

Auditory-based defence against gleaning bats in neotropical katydids (Orthoptera: Tettigoniidae)

Neotropical katydids (Orthoptera: Tettigoniidae) are preyed on by gleaning bats, which are known to use male calling songs to locate them. At least one katydid species has been reported to stop singing in response to bat echolocation calls. To investigate the relationship between this behavioural defence and ecological and sensory factors, we surveyed calling song characteristics, song cessation in response to the echolocation calls of a sympatric gleaning bat (Trachops cirrhosus), and T-cell responses (an auditory interneuron sensitive to ultrasound) in five katydid species from Panamá. The two katydid species that stopped singing in response to bat calls (Balboa tibialis and Ischnomela gracilis, Pseudophyllinae) also had the highest T-cell spike number and rate in response to these stimuli. The third pseudophylline species (Docidocercus gigliotosi) did not reliably cease singing and had low T-cell spiking activity. Neoconocephalus affinis (Copiphorinae) produced continuous calling song, possibly preventing males from hearing the bat during singing, and did not show a behavioural response despite high T-cell activity in response to bat calls. Steirodon rufolineatum (Phaneropterinae) did not cease singing and differed in T-cell activity compared to the other species. T-cell function might not be conserved in katydids, and evidence for this idea is discussed.     

Distress Calls of a Fast-Flying Bat (Molossus molossus) Provoke Inspection Flights but Not Cooperative Mobbing

Many birds and mammals produce distress calls when captured. Bats often approach speakers playing conspecific distress calls, which has led to the hypothesis that bat distress calls promote cooperative mobbing. An alternative explanation is that approaching bats are selfishly assessing predation risk. Previous playback studies on bat distress calls involved species with highly maneuverable flight, capable of making close passes and tight circles around speakers, which can look like mobbing. We broadcast distress calls recorded from the velvety free-tailed bat, Molossus molossus, a fast-flying aerial-hawker with relatively poor maneuverability. Based on their flight behavior, we predicted that, in response to distress call playbacks, M. molossus would make individual passing inspection flights but would not approach in groups or approach within a meter of the distress call source. By recording responses via ultrasonic recording and infrared video, we found that M. molossus, and to a lesser extent Saccopteryx bilineata, made more flight passes during distress call playbacks compared to noise. However, only the more maneuverable S. bilineata made close approaches to the speaker, and we found no evidence of mobbing in groups. Instead, our findings are consistent with the hypothesis that single bats approached distress calls simply to investigate the situation. These results suggest that approaches by bats to distress calls should not suffice as clear evidence for mobbing.