Frugivorous Bats Research Articles

Not all farms are created equal: Shady African cocoa farms promote a richer bat fauna

Bats provide important pest suppression services with economic value to cocoa farmers, yet the impact of cocoa farm management on bat diversity metrics is still poorly understood. This is especially important if we consider that Afrotropical cocoa farms supply 68 % of the world's chocolate market, with expected increases in production in the forthcoming decades. In this study, we investigated for the first time how bat abundance, richness and diversity varied between African cocoa farms with different levels of shade tree cover, shade tree communities and cocoa characteristics. We found that shade tree cover and shade tree height were the main drivers associated with an increase of Shannon diversity, and abundance and richness of insectivores. Frugivorous and nectarivorous bats were positively associated with the presence of planted shade trees, but richness varied with the size of shade trees. The insectivorous Hipposideros fuliginosus was only present in high shade farms, being captured 51 times only in this shade system, while the frugivorous Myonycteris angolensis was associated with low shade farms. Our findings show that indeed not all farms are created equal, with high shade farms with large, tall forest shade trees (i.e., containing key plant resources) having richer bat communities. Therefore, policymakers seeking to conserve wildlife within cocoa farming systems should adopt cocoa management systems like those mentioned above and promote a combination of forest and planted shade trees to be able support a rich community of insectivorous, frugivorous and nectarivorous bats and maintain their associated ecosystems services.

Characterizing the blood microbiota of omnivorous and frugivorous bats (Chiroptera: Phyllostomidae) in Casanare, eastern Colombia.

Bats are known reservoirs of seemingly-innocuous pathogenic microorganisms (including viruses, bacteria, fungi, and protozoa), which are associated with triggering disease in other zoonotic groups. The taxonomic diversity of the bats' microbiome is likely associated with species-specific phenotypic, metabolic, and immunogenic capacities. To date, few studies have described the diversity of bat blood microbial communities. Then, this study used amplicon-based next generation sequencing of the V4 hypervariable region of the 16S-rRNA gene in blood samples from omnivorous (n = 16) and frugivorous (n = 9) bats from the department of Casanare in eastern Colombia. We found the blood microbiota in bats to be composed of, among others, Bartonella and Mycoplasma bacterial genera which are associated with various disease phenotypes in other mammals. Furthermore, our results suggest that the bats' dietary habits might determine the composition and the persistence of some pathogens over others in their bloodstream. This study is among the first to describe the blood microbiota in bats, to reflect on co-infection rates of multiple pathogens in the same individual, and to consider the influence of diet as a factor affecting the animal's endogenous microbial community.

The tongue morphology of Pteropus vampyrus from Timor Island, Indonesia: New insights from scanning electron and light microscopic studies

Abstract. Selan YN, Wihadmadyatami H, Haryanto A, Kusindarta DL. 2023. The tongue morphology of Pteropus vampyrus from Timor Island, Indonesia: New insights from scanning electron and light microscopic studies. Biodiversitas 24: 3512-3518. The large flying fox (Pteropus vampyrus Linnaeus, 1758) is a Southeast Asian megabat species includes with frugivorous bats. The tongue plays a pivotal role in taking, chewing, and swallowing food. The structure of the bat tongue hampers considerable variation, mainly in the papilla. Variations occur owing to the feeding habits, environment, and adaptation of bats to their environments. The aim of this study was to clarify the morphological structure of the tongue of P. vampyrus obtained from the island of Timor, East Nusa Tenggara, Indonesia, by using Scanning Electron Microscope (SEM) and Light Microscopy(LM). This study included six adult bats regardless of sex. Macroscopically, the tongue of P. vampyrus consists of three parts: the apex, corpus, and radix. SEM and LM confirmed that the apex presents filiform papillae of several subtypes, including scale-like filiform, giant trifid, and small crown-like papillae. In addition, the apex features fungiform and transitional papillae between the giant trifid and small crown-like papillae. Furthermore, the corpus consists of filiform papillae (leaf-like filiform and large crown-like papillae) and fungiform papillae. The radix consists of filiform papillae (long conical, leaf-like filiform, and short conical papillae), fungiform papillae, and three V-shaped circumvallate papillae pointing to the larynx.

Diet and the evolution of ADH7 across seven orders of mammals

Dietary variation within and across species drives the eco-evolutionary responsiveness of genes necessary to metabolize nutrients and other components. Recent evidence from humans and other mammals suggests that sugar-rich diets of floral nectar and ripe fruit have favoured mutations in, and functional preservation of, the ADH7 gene, which encodes the ADH class 4 enzyme responsible for metabolizing ethanol. Here we interrogate a large, comparative dataset of ADH7 gene sequence variation, including that underlying the amino acid residue located at the key site (294) that regulates the affinity of ADH7 for ethanol. Our analyses span 171 mammal species, including 59 newly sequenced. We report extensive variation, especially among frugivorous and nectarivorous bats, with potential for functional impact. We also report widespread variation in the retention and probable pseudogenization of ADH7 . However, we find little statistical evidence of an overarching impact of dietary behaviour on putative ADH7 function or presence of derived alleles at site 294 across mammals, which suggests that the evolution of ADH7 is shaped by complex factors. Our study reports extensive new diversity in a gene of longstanding ecological interest, offers new sources of variation to be explored in functional assays in future study, and advances our understanding of the processes of molecular evolution.

Auditory brainstem response recovery from forward masking in insectivorous and frugivorous bats

Echolocating bats rely on precise temporal processing of sound, as echolocation calls may be emitted at rates as high as 150–200 sounds per second in the terminal “buzz” phase that precedes prey capture by insectivorous species. High call repetition rates could introduce forward masking effects that interfere with echo detection; however, echolocating bats may have evolved auditory specializations to prevent repetition suppression of auditory responses and facilitate detection of sounds separated by very brief time intervals. We assessed the time course of post-stimulus recovery of the auditory brainstem response (ABR) in two bat species that differ in the temporal characteristics of their sonar behaviors: the insectivorous Eptesicus fuscus, which uses high sonar call rates to capture prey and the frugivorous Carollia perspicillata, which uses lower call rates to forage. We recorded forward-masking ABRs to paired clicks at varied inter-stimulus intervals and measured recovery from prior stimulation as the ratio of response amplitudes and latencies evoked by the second stimulus relative to the first. We observed significant species-specific effects of forward masking on ABR responses in which E. fuscus maintained comparable responses to ISIs less than 4 ms compared to longer post-stimulus response recovery times (>6 ms) in C. perspicillata.

Between wrinkles and stripes: the enigma of the old centurion

The wrinkle-faced bat (Centurio senex) is a rarely captured, frugivorous bat species – which is also a seed predator – distributed across Central America and northern South America. Despite purportedly having the strongest bite force within members of the Phyllostomidae family, little else is known about aspects of this bat's natural history, including which fruits and seeds it prefers. Among the 226 described species in the Phyllostomidae, C senex is unique in appearance, with (as its common name suggests) a wrinkled face and with striped, partly translucent wings. The wrinkles have been hypothesized to help the bat direct juice extracted from fruits into its mouth, or to assist with navigation through echolocation. However, evidence to support either statement has so far not been found.

Spatial learning overshadows learning novel odors and sounds in both predatory and frugivorous bats

Abstract To forage efficiently, animals should selectively attend to and remember the cues of food that best predict future meals. One hypothesis is that animals with different foraging strategies should vary in their reliance on spatial versus feature cues. Specifically, animals that store food in dispersed caches or that feed on spatially stable food, such as fruits or flowers, should be relatively biased towards learning a meal’s location, whereas predators that hunt mobile prey should instead be relatively biased towards learning feature cues such as odor or sound. Several authors have predicted that nectar-feeding and fruit-feeding bats would rely relatively more on spatial cues, whereas closely related predatory bats would rely more on feature cues, yet no experiment has compared these two foraging strategies under the same conditions. To test this hypothesis, we compared learning in the frugivorous bat, Artibeus jamaicensis, and the predatory bat, Lophostoma silvicolum, which hunts katydids using acoustic cues. We trained bats to find food paired with a unique and novel odor, sound, and location. To assess which cues each bat had learned, we then dissociated these cues to create conflicting information. Rather than finding that the frugivore and predator clearly differ in their relative reliance on spatial versus feature cues, we found that both species used spatial cues over sounds or odors in subsequent foraging decisions. We interpret these results alongside past findings on how foraging animals use spatial cues versus feature cues, and explore why spatial cues may be fundamentally more rich, salient, or memorable.

DIVERSIDAD DE MURCIÉLAGOS FRUGÍVOROS Y SEMILLAS CONSUMIDAS EN BORDES DE BOSQUE MESÓFILO DE MONTAÑA, VERACRUZ, MÉXICO

<p><strong>Background: </strong>The change in the coverage of the Cloud Forest (CF) generates edges and fragments of original vegetation that can affect the bat community and the diversity of dispersed seeds. <strong>Objective:</strong> The objective was to describe the diversity of frugivorous bats and the seeds that they consume in different types of edges in the BMM, in Huatusco, Veracruz, Mexico. <strong>Methodology:</strong> Sampling with nets every 28 days for the capture and identification of bats was carried out in seven months, their feces were collected and the contained seeds were germinated to estimate a germination rate and for their taxonomic identification. The bat community and the seeds consumed were evaluated with true diversity indicators; the disperser importance index (IID) was estimated with the percentage of seeds dispersed by bat species. <strong>Results:</strong> 503 individuals of 14 species of frugivorous bats were captured in the four borders of the BMM, but the highest presence (13 spp.) and abundance (60%) of frugivorous-polynectarivorous bats was recorded in the border of the BMM with Grassland, where <em>Anoura geoffroyi</em>, <em>Sturnira ludovici</em> and <em>S. lilium</em> had the highest abundance, but only three species of bats are dispersal agents. A total of 69 bat droppings with 1380 seeds belonging to four botanical families were collected, with Rubiaceae and Solanaceae having the highest frequency of seeds consumed, and Piperaceae and Solanaceae with the greatest diversity of seeds. The highest quantity (65%) and diversity of seeds (10 spp.) were recorded on the BMM-Grassland border, with <em>Borreria laevis</em> seeds being the most consumed (30%). <strong>Implications: </strong>This study allows us to understand the ecological importance of biotic interactions between bats and plants in BMM borders. <strong>Conclusions:</strong> The edges of heterogeneous BMM conglomerate greater diversity and abundance of bats.</p>

Identification of coronaviruses in bats and rodents in northern and central Argentina.

Due to the present pandemic situation and the many animal species that are epidemiologically involved, there has been a surge of renewed interest in investigating the coronavirus (CoV) population circulating in wildlife, especially bats and rodents, which are potential reservoirs of new human pathogens. In Argentina, information about the viruses present in these mammals is very limited. To investigate the presence of coronaviruses in this country, we obtained 457 samples from hematophagous, insectivorous, and frugivorous bats and rodents from two regions of Argentina. We report here the detection of alphacoronavirus sequences in three groups of bats as well as in rodents. Phylogenetic analysis showed the closest relationships to alphacoronaviruses from Brazil.

Morphological, Anatomical, and Physiological Signs of Senescence in the Great Fruit-Eating Bat (Artibeus lituratus)

The longevity of bats is longer than expected based on their small body sizes and high metabolic rate. However, signs of senescence have been poorly studied for free-living bats, especially for Neotropical species, because elderly individuals are challenging to find in the wild, and long-term mark-recapture studies are lacking. Here, we present the first record of a free-living Neotropical frugivorous bat, a female Artibeus lituratus (family Phyllostomidae), with impressive signs of senescence. We compare the elderly bat with conspecific juveniles and non-elderly adults morphologically, anatomically, and physiologically. The most noticeable signs of senescence were a significant loss of fur, dark spots on the skin, excessive dental wear, and reduced ability to assimilate sugar. These traits indicate that bats' challenges as they get old can be associated with reduced thermal insulation, ability to chew, and nutrient assimilation. However, by reducing extrinsic causes of mortality, flying capability in old bats with clear signs of senescence may represent a vital survival trait associated with the long lifespan of these animals.

Coronaviruses Are Abundant and Genetically Diverse in West and Central African Bats, including Viruses Closely Related to Human Coronaviruses.

Bats are at the origin of human coronaviruses, either directly or via an intermediate host. We tested swabs from 4597 bats (897 from the Democratic Republic of Congo (DRC), 2191 from Cameroon and 1509 from Guinea) with a broadly reactive PCR in the RdRp region. Coronaviruses were detected in 903 (19.6%) bats and in all species, with more than 25 individuals tested. The highest prevalence was observed in Eidolon helvum (239/733; 39.9%) and Rhinolophus sp. (306/899; 34.1%), followed by Hipposideros sp. (61/291; 20.9%). Frugivorous bats were predominantly infected with beta coronaviruses from the Nobecovirus subgenus (93.8%), in which at least 6 species/genus-specific subclades were observed. In contrast, insectivorous bats were infected with beta-coronaviruses from different subgenera (Nobecovirus (8.5%), Hibecovirus (32.8%), Merbecovirus (0.5%) and Sarbecovirus (57.6%)) and with a high diversity of alpha-coronaviruses. Overall, our study shows a high prevalence and genetic diversity of coronaviruses in bats and illustrates that Rhinolophus bats in Africa are infected at high levels with the Sarbecovirus subgenus, to which SARS-CoV-2 belongs. It is important to characterize in more detail the different coronavirus lineages from bats for their potential to infect human cells, their evolution and to study frequency and modes of contact between humans and bats in Africa.

Rabies in Bats (Chiroptera, Mammalia) in Brazil: Prevalence and Potential Risk Factors Based on Twenty Years of Research in the Northwestern Region of São Paulo, Brazil

The number of rabies cases in bats has increased recently in Brazil and in the state of São Paulo, representing a new epidemiological scenario for this zoonosis. This study aimed to analyze the prevalence of rabies in bats according to food habits, taxonomic classification, sex and season of the year to identify possible risk factors for rabies occurrence in bats. A retrospective analysis of 6389 records of bat samples, from different municipalities of São Paulo, submitted to rabies diagnosis and taxonomic identification was carried out at the Rabies Diagnostic and Chiroptera Laboratories of Unesp Araçatuba, São Paulo, Brazil, from 1998 to 2017. Seventy-six (1.1%) positive rabies cases were detected in bats from ten species and seven genera of three families. The number of rabies-positive cases was higher in the dry season, with a significant association. The prevalence was higher in the Vespertilionidae family (37), especially Myotis nigricans (19) and Eptesicus furinalis (14). Frugivorous bats had a greater association with positivity for rabies, whereas the variable "sex" had no association. We recommend that the surveillance and control of rabies should be undertaken primarily during the dry season, especially in the Vespertilionidae family species and other species with a frugivorous food habit.

Glyphosate Alters Redox Balance and Induces Histomorphological Alterations in the Testes of Fruit-Eating Bats (Artibeus lituratus)

We investigate the effects of Glyphosate (GLY) on the testes of fruit-eating bats (Artibeus lituratus). Our study aimed to evaluate the effects of short-time exposure to GLY herbicide on adult male bats testes. Adult male bats were exposed for three days: Control (fed fresh fruits) and GLY (fed 4 mL / 100 mL GLY-pulverized fruit). Animals fed with contaminated fruits showed a reduction in body mass. Antioxidant enzyme catalase (CAT) activity and carbonylated protein (PCN) levels increased in the teste’s GLY-exposed bats. Histomorphometry revealed an increase in the luminal parameters as well as in the epithelium tubule ratio, which is indicative of a reduction in epithelium area. There was also an increase in the percentage of macrophages and a decrease in the percentage and number of Leydig cells. The results indicate that short term exposure to GLY in frugivorous bats may cause oxidative stress of the tissue that possibly induces testicular morphological changes that may compromise the reproduction and maintenance of the species.

Exposure of Egyptian Rousette Bats (Rousettus aegyptiacus) and a Little Free-Tailed Bat (Chaerephon pumilus) to Alphaviruses in Uganda.

The reservoir for zoonotic o'nyong-nyong virus (ONNV) has remained unknown since this virus was first recognized in Uganda in 1959. Building on existing evidence for mosquito blood-feeding on various frugivorous bat species in Uganda, and seroprevalence for arboviruses among bats in Uganda, we sought to assess if serum samples collected from bats in Uganda demonstrated evidence of exposure to ONNV or the closely related zoonotic chikungunya virus (CHIKV). In total, 652 serum samples collected from six bat species were tested by plaque reduction neutralization test (PRNT) for neutralizing antibodies against ONNV and CHIKV. Forty out of 303 (13.2%) Egyptian rousettes from Maramagambo Forest and 1/13 (8%) little free-tailed bats from Banga Nakiwogo, Entebbe contained neutralizing antibodies against ONNV. In addition, 2/303 (0.7%) of these Egyptian rousettes contained neutralizing antibodies to CHIKV, and 8/303 (2.6%) contained neutralizing antibodies that were nonspecifically reactive to alphaviruses. These data support the interepidemic circulation of ONNV and CHIKV in Uganda, although Egyptian rousette bats are unlikely to serve as reservoirs for these viruses given the inconsistent occurrence of antibody-positive bats.

BATS OF PULAU TINGGI, JOHOR, MALAYSIA

A series of bat surveys took place in Pulau Tinggi from July 2019 to September 2019. A total of 242 individuals representing 15 species from six families were captured from a cumulative effort of 462 trap nights. The most caught species for frugivorous bats was Cynopterus brachyotis (n = 150) while for insectivorous bats, it was Hipposideros cervinus (n = 20). Pulau Tinggi has a high density of bat species per area (1.01 sp/km2) when compared to other tourist islands on Peninsular Malaysia’s east coast [e.g., Pulau Tioman (0.13 sp/km2), Pulau Perhentian (0.5 sp/km2) and Pulau Redang (0.4 sp/km2)]. As a result, high levels of disturbance such as tourism and habitat loss may negatively affect the diversity of bat species on the island. Because of time constraints and the study did not cover the entire island, information on the diversity of bats in Pulau Tinggi is still inadequate. Long-term monitoring of bat diversity covering forest areas throughout the island needs to be conducted immediately to identify the number of species, their distribution and ecology. This information is important in formulating a strategic plan for bat conservation in Pulau Tinggi.

Eat what you can, when you can: relatively high arthropod consumption by frugivorous bats in Amazonian Peru

Eat what you can, when you can: relatively high arthropod consumption by frugivorous bats in Amazonian Peru

Effect of artificial light on activity in frugivorous bats (Pteropodidae)

Effect of artificial light on activity in frugivorous bats (Pteropodidae)

Configuration and composition of human-dominated tropical landscapes affect the prevalence and average intensity of mite and fly infestation in Phyllostomidae bats.

The conversion of natural areas into agricultural landscapes results in different mosaics of land use types, modifying biodiversity and consequently altering the patterns of ecological interactions, such as between frugivorous bats and ectoparasites. Our objectives were to investigate whether variations in the configuration and composition of human-disturbed landscapes interfere with the prevalence and average intensity of ectoparasite infestation in the frugivorous bats Artibeus lituratus (Olfers, 1818), Carollia perspicillata (Linnaeus, 1758), and Sturnira lilium (É Geoffroy, 1810), in a region of the Brazilian Atlantic Forest. We also evaluated whether there is a response in the parasite load associated with the ectoparasite group (mite or fly). We found six species of flies and three mites. The proportion of infested hosts was more affected by the landscape than the mean infestation values. Land cover diversity influenced seven of the interactions studied. Forest cover affected eight of the interactions and was associated with a reduction in the parasite load in seven of them. The increase in the proportion of edges per area of each fragment presented a different influence related to the host species. Variations in parasite load did not show any typical response related to the mite or fly group. Our study indicates that landscape configuration and composition interfere with bat-ectoparasite interactions, which may be related to interference in encounter rates between hosts (for mites and flies) and between hosts and their ectoparasites in roosts (for flies). The taxonomic identity of the interacting species suggests that the relationship with the landscape is context-dependent.

Influence of landscape ecology and physiological implications in bats from different trophic guilds

Bats may serve as bioindicators of human impact on landscape ecology. This study aimed to evaluate the health condition of bats from different food guilds captured in two areas with different land use profiles in Brazil and to compare data on the oxidant-antioxidant balance and histopathological changes due to different anthropogenic pressures. Bats were collected from a protected area in Serra do Cipó National Park (SCNP), MG, Brazil, and an area with intense agricultural activity in the municipality of Uberaba (UB), MG, Brazil. Despite the differences in land use and occupation between the studied areas, bats showed similar responses. However, the trophic guilds were affected differently. Frugivorous bats in both areas showed lower activities of the enzymes superoxide dismutase (SOD), catalase (CAT), and glutathione S-transferase (GST) and concentrations of malondialdehyde (MDA) than other guilds, which can be explained by the greater intake of antioxidants from the diet in addition to the lower production of reactive oxygen species (ROS). Histopathological analysis of the livers revealed that the animals had a similar prevalence in the two areas, with some differences related to guilds. Compared with other bats, hematophagous bats from SCNP had a higher prevalence of steatosis and, together with frugivorous bats from Uberaba, had higher frequencies of ballooning degeneration, suggesting that these animals are subjected to anthropogenic factors capable of inducing disturbances in hepatic metabolism. Hematophagous bats from Uberaba had a higher prevalence of portal inflammation, while insectivorous bats from Uberaba had a higher prevalence of lobular and portal inflammation. The profiles of use and occupation of the areas are different; Uberaba bats seem to face worse conditions because they show more liver damage owing to lipoperoxidation.

Detection of Alpha- and Betacoronaviruses in Frugivorous and Insectivorous Bats in Nigeria

The rise of bat-associated zoonotic viruses necessitates a close monitoring of their natural hosts. Since the detection of severe acute respiratory syndrome coronavirus (SARS-CoV), it is evident that bats are vital reservoirs of coronaviruses (CoVs). In this study, we investigated the presence of CoVs in multiple bat species in Nigeria to identify viruses in bats at high-risk human contact interfaces. Four hundred and nine bats comprising four bat species close to human habitats were individually sampled from five states in Nigeria between 2019 and 2021. Coronavirus detection was done using broadly reactive consensus PCR primers targeting the RNA-dependent RNA polymerase (RdRp) gene of CoVs. Coronavirus RNA was detected in 39 samples (9.5%, CI 95%: [7.0, 12.8]), of which 29 were successfully sequenced. The identified CoVs in Nigerian bats were from the unclassified African alphacoronavirus lineage and betacoronavirus lineage D (Nobecovirus), with one sample from Hipposideros ruber coinfected with alphacoronavirus and betacoronavirus. Different bat species roosting in similar or other places had CoVs from the same genetic lineage. The phylogenetic and evolutionary dynamics data indicated a high CoV diversity in Nigeria, while host switching may have contributed to CoV evolution. Robust sentinel surveillance is recommended to enhance our knowledge of emerging and re-emerging coronaviruses.