Calling to the collective: contact calling rates within groups of disc-winged bats do not vary by kinship or association.

Many group-living animals coordinate social behaviours using contact calls, which can be produced for all group members or targeted at specific individuals. In the disc-winged bat, Thyroptera tricolor, group members use 'inquiry' and 'response' calls to coordinate daily movements into new roosts (furled leaves). Rates of both calls show consistent among-individual variation, but causes of within-individual variation remain unknown. Here, we tested whether disc-winged bats produce more contact calls towards group members with higher kinship or association. In 446 experimental trials, we recorded 139 random within-group pairs of one flying bat (producing inquiry calls for roost searching) and one roosting bat (producing response calls for roost advertising). Using generalized linear mixed-effect models (GLMM), we assessed how response and inquiry calling rates varied by sender, receiver, genetic kinship and co-roosting association rate. Calling rates varied consistently across senders but not by receiver. Response calling was influenced by inquiry calling rates, but neither calling rate was higher when the interacting pair had higher kinship or association. Rather than dyadic calling rates indicating within-group relationships, our findings are consistent with the hypothesis that bats produce contact calls to maintain contact with any or all individuals within a group while collectively searching for a new roost site. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

Group vocal composition and decision-making during roost finding in Spix's disk-winged bats.

Theoretical work suggests that having many informed individuals within social groups can promote efficient resource location. However, it may also give rise to group fragmentation if members fail to reach consensus on their direction of movement. In this study, we investigate whether the number of informed individuals, exemplified by bats emitting calls from different roosts, influences group cohesion in Spix's disk-winged bats (Thyroptera tricolor). Additionally, we explore the role of signal reliability, quantified through signalling rates, in group consensus on where to roost. These bats use contact calls to announce the location of a roost site and recruit conspecifics. The groups they form exhibit high levels of cohesion and consist of both vocal and non-vocal bats, with vocal behaviour being consistent over time. Our findings revealed that an increase in the number of roosts broadcasting calls is strongly associated with the likelihood of groups fragmenting among multiple roosts. Additionally, we found that a majority of group members enter the roost with higher calling rates. This phenomenon can mitigate the risk of group fragmentation, as bats emitting more calls may contribute to greater group consensus on roosting locations, thereby reducing the likelihood of individuals separating and enhancing overall group cohesion. Our results highlight the potential costs of having too many information producers for group coordination, despite their established role in finding critical resources. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

Landing manoeuvres predict roost-site preferences in bats.

Roosts are vital for the survival of many species, and how individuals choose one site over another is affected by various factors. In bats, for example, species may use stiff roosts such as caves or compliant ones such as leaves; each type requires not only specific morphological adaptations but also different landing manoeuvres. Selecting a suitable roost within those broad categories may increase landing performance, reducing accidents and decreasing exposure time to predators. We addressed whether bats select specific roost sites based on the availability of a suitable landing surface, which could increase landing performance. Our study focused on Spix's disc-winged bats (Thyroptera tricolor), a species known to roost within developing tubular leaves. As previous studies show that this species relies on the leaves' apex for safe landing and rapid post-landing settlement, we predicted that bats would prefer to roost in tubular structures with a longer apex and that landing would be consistently more effective on those leaves. Field observations showed that T. tricolor predominantly used two species for roosting, Heliconia imbricata and Calathea lutea, but they preferred roosting in the former. The main difference between these two plant species was the length of the leaf's apex (longer in H. imbricata). Experiments in a flight cage also showed that bats used more consistent approach and landing tactics when accessing leaves with a longer apex. Our results suggest that landing mechanics may strongly influence resource selection, especially when complex manoeuvres are needed to acquire those resources.

Bats mimic hymenopteran insect sounds to deter predators.

Mimicry is one of the most fascinating phenomena in nature1. Mimicry traits often reflect complex, finely tuned, and sometimes extravagant relationships among species and have evolved to deceive predators or prey. Indeed, mimicry has most often evolved to discourage predation: the 'mimic' exhibits phenotypic convergence towards a non-related 'model' organism which is inedible or harmful, so that a given predator, or 'receiver', will refrain from attacking or ingesting the mimic. Traditionally, mimicry is mainly evident and has been mainly studied in the visual domain. Here, we report experiments that document the first case of interspecific acoustic mimicry in a mammal and demonstrate that the distress calls the greater mouse-eared bat (Myotis myotis) broadcasts when handled imitate sounds of stinging bees or wasps to discourage the bat's avian predators.

Fungal communities in feces of the frugivorous bat Ectophylla alba and its highly specialized Ficus colubrinae diet.

BACKGROUND: Bats are important long-distance dispersers of many tropical plants, yet, by consuming fruits, they may disperse not only the plant's seeds, but also the mycobiota within those fruits. We characterized the culture-dependent and independent fungal communities in fruits of Ficus colubrinae and feces of Ectophylla alba to determine if passage through the digestive tract of bats affected the total mycobiota. RESULTS: Using presence/absence and normalized abundance data from fruits and feces, we demonstrate that the fungal communities were significantly different, even though there was an overlap of ca. 38% of Amplicon Sequence Variants (ASVs). We show that some of the fungi from fruits were also present and grew from fecal samples. Fecal fungal communities were dominated by Agaricomycetes, followed by Dothideomycetes, Sordariomycetes, Eurotiomycetes, and Malasseziomycetes, while fruit samples were dominated by Dothideomycetes, followed by Sordariomycetes, Agaricomycetes, Eurotiomycetes, and Laboulbeniomycetes. Linear discriminant analyses (LDA) show that, for bat feces, the indicator taxa include Basidiomycota (i.e., Agaricomycetes: Polyporales and Agaricales), and the ascomycetous class Eurotiomycetes (i.e., Eurotiales, Aspergillaceae). For fruits, indicator taxa are in the Ascomycota (i.e., Dothideomycetes: Botryosphaeriales; Laboulbeniomycetes: Pyxidiophorales; and Sordariomycetes: Glomerellales). In our study, the differences in fungal species composition between the two communities (fruits vs. feces) reflected on the changes in the functional diversity. For example, the core community in bat feces is constituted by saprobes and animal commensals, while that of fruits is composed mostly of phytopathogens and arthropod-associated fungi. CONCLUSIONS: Our study provides the groundwork to continue disentangling the direct and indirect symbiotic relationships in an ecological network that has not received enough attention: fungi-plants-bats. Findings also suggest that the role of frugivores in plant-animal mutualistic networks may extend beyond seed dispersal: they may also promote the dispersal of potentially beneficial microbial symbionts while, for example, hindering those that can cause plant disease.

Functional correlates of skull shape in Chiroptera: feeding and echolocation adaptations.

Morphological, functional, and behavioral adaptations of bats are among the most diverse within mammals. A strong association between bat skull morphology and feeding behavior has been suggested previously. However, morphological variation related to other drivers of adaptation, in particular echolocation, remains understudied. We assessed variation in skull morphology with respect to ecology (diet and emission type) and function (bite force, masticatory muscles and echolocation characteristics) using geometric morphometrics and comparative methods. Our study suggests that variation in skull shape of 10 bat families is the result of adaptations to broad dietary categories and sound emission types (oral or nasal). Skull shape correlates with echolocation parameters only in a subsample of insectivorous species, possibly because they (almost) entirely rely on this sensory system for locating and capturing prey. Insectivores emitting low frequencies are characterized by a ventrally tilted rostrum, a trait not associated with feeding parameters. This result questions the validity of a trade-off between feeding and echolocation function. Our study advances understanding of the relationship between skull morphology and specific features of echolocation and suggests that evolutionary constraints due to echolocation may differ between different groups within the Chiroptera.

Comparing the efficiency of monofilament and regular nets for capturing bats.

Regular nylon or polyester mist nets used for capturing bats have several drawbacks, particularly that they are inefficient at sampling insectivorous species. One possible alternative is to use monofilament nets, whose netting is made of single strands of yarn instead of several as regular nets, making them less detectable. To date, only one study has quantified the differences in capture rates between monofilament and regular mist nets for the study of bats, yet surprisingly, its findings suggest that the latter are more efficient than the former. Here, we provide further evidence of the differences in sampling efficiency between these two nets. We captured 90 individuals and 14 species in regular nets and 125 individuals and 20 species in monofilament nets. The use of monofilament nets increased overall capture rates, particularly for insectivorous species. Species accumulation curves indicate that samples based on regular nets are significantly underestimating species diversity, most notably as these nets fail at sampling rare species. We show that incorporating monofilament nets into bat studies offers an opportunity to expand records of different guilds and rare bat species and to improve our understanding of poorly known bat assemblages while using a popular, relatively cheap and portable sampling method.

The role of the gut microbiota in the dietary niche expansion of fishing bats.

BACKGROUND: Due to its central role in animal nutrition, the gut microbiota is likely a relevant factor shaping dietary niche shifts. We analysed both the impact and contribution of the gut microbiota to the dietary niche expansion of the only four bat species that have incorporated fish into their primarily arthropodophage diet. RESULTS: We first compared the taxonomic and functional features of the gut microbiota of the four piscivorous bats to that of 11 strictly arthropodophagous species using 16S rRNA targeted amplicon sequencing. Second, we increased the resolution of our analyses for one of the piscivorous bat species, namely Myotis capaccinii, and analysed multiple populations combining targeted approaches with shotgun sequencing. To better understand the origin of gut microorganisms, we also analysed the gut microbiota of their fish prey (Gambusia holbrooki). Our analyses showed that piscivorous bats carry a characteristic gut microbiota that differs from that of their strict arthropodophagous counterparts, in which the most relevant bacteria have been directly acquired from their fish prey. This characteristic microbiota exhibits enrichment of genes involved in vitamin biosynthesis, as well as complex carbohydrate and lipid metabolism, likely providing their hosts with an enhanced capacity to metabolise the glycosphingolipids and long-chain fatty acids that are particularly abundant in fish. CONCLUSIONS: Our results depict the gut microbiota as a relevant element in facilitating the dietary transition from arthropodophagy to piscivory.

The energetics of social signaling during roost location in Spix's disc-winged bats.

Long-term social aggregations are maintained by multiple mechanisms, including the use of acoustic signals, which may nonetheless entail significant energetic costs. To date, however, no studies have gauged whether there are significant energetic costs to social call production in bats, which heavily rely on acoustic communication for a diversity of social tasks. We measured energetic expenditure during acoustic signaling in Spix's disc-winged bats (Thyroptera tricolor), a species that commonly uses contact calls to locate the ephemeral furled leaves that they use for roosting. To determine the cost of sound production, we measured oxygen consumption using intermittent-flow respirometry methods, with and without social signaling. Our results show that the emission of contact calls significantly increases oxygen consumption; vocal individuals spent, on average, 12.42 kJ more during social signaling trials than they spent during silent trials. We also found that as resting metabolic rate increased in males, there was a decreasing probability that they would emit response calls. These results provide support to the 'allocation model', which predicts that only individuals with lower self-maintenance costs can afford to spend energy in additional activities. Our results provide a step forward in our understanding of how physiology modulates behavior, specifically how the costs of call production and resting metabolic rate may explain the differences in vocal behavior among individuals.

Specialized landing maneuvers in Spix's disk-winged bats (Thyroptera tricolor) reveal linkage between roosting ecology and landing biomechanics.

Disk-winged bats (Thyroptera spp.) are the only mammals that use suction to cling to smooth surfaces, having evolved suction cups at the bases of the thumbs and feet that facilitate attachment to specialized roosts: the protective funnels of ephemeral furled leaves. We predicted that this combination of specialized morphology and roosting ecology is coupled with concomitantly specialized landing maneuvers. We tested this by investigating landings in Thyroptera tricolor using high-speed videography and a force-measuring landing pad disguised within a furled leaf analogue. We found that their landing maneuvers are distinct among all bats observed to date. Landings comprised three phases: (1) approach, (2) ballistic descent and (3) adhesion. During approach, bats adjusted trajectory until centered in front of and above the landing site, typically the leaf's protruding apex. Bats initiated ballistic descent by arresting the wingbeat cycle and tucking their wings to descend toward the leaf, simultaneously extending the thumb disks cranially. Adhesion commenced when the thumb disks contacted the landing site. Significant body reorientation occurred only during adhesion, and only after contact, when the thumb disks acted as fulcra about which the bats pitched 75.02±26.17 deg (mean±s.d.) to swing the foot disks into contact. Landings imposed 6.98±1.89 bodyweights of peak impact force. These landing mechanics are likely to be influenced by the orientation, spatial constraints and compliance of furled leaf roosts. Roosting ecology influences critical aspects of bat biology, and taken as a case study, this work suggests that roosting habits and landing mechanics could be functionally linked across bats.

Social communication in bats.

Bats represent one of the most diverse mammalian orders, not only in terms of species numbers, but also in their ecology and life histories. Many species are known to use ephemeral and/or unpredictable resources that require substantial investment to find and defend, and also engage in social interactions, thus requiring significant levels of social coordination. To accomplish these tasks, bats must be able to communicate; there is now substantial evidence that demonstrates the complexity of bat communication and the varied ways in which bats solve some of the problems associated with their unique life histories. However, while the study of communication in bats is rapidly growing, it still lags behind other taxa. Here we provide a comprehensive overview of communication in bats, from the reasons why they communicate to the diversity and application of different signal modalities. The most widespread form of communication is the transmission of a signaller's characteristics, such as species identity, sex, individual identity, group membership, social status and body condition, and because many species of bats can rely little on vision due to their nocturnal lifestyles, it is assumed that sound and olfaction are particularly important signalling modes. For example, research suggests that secretions from specialized glands, often in combination with urine and saliva, are responsible for species recognition in several species. These olfactory signals may also convey information about sex and colony membership. Olfaction may be used in combination with sound, particularly in species that emit constant frequency (CF) echolocation calls, to recognize conspecifics from heterospecifics, yet their simple structure and high frequency do not allow much information of individual identity to be conveyed over long distances. By contrast, social calls may encode a larger number of cues of individual identity, and their lower frequencies increase their range of detection. Social calls are also known to deter predators, repel competitors from foraging patches, attract group mates to roost sites, coordinate foraging activities, and are used during courtship. In addition to sound, visual displays such as wing flapping or hovering may be used during courtship, and swarming around roost sites may serve as a visual cue of roost location. However, visual communication in bats still remains a poorly studied signal modality. Finally, the most common form of tactile communication known in bats is social grooming, which may be used to signal reproductive condition, but also to facilitate and strengthen cooperative interactions. Overall, this review demonstrates the rapid advances made in the study of bat social communication during recent years, and also identifies topics that require further study, particularly those that may allow us to understand adaptation to rapidly changing environmental conditions.

Variation in echolocation call frequencies in two species of free-tailed bats according to temperature and humidity.

Bats can actively adjust their echolocation signals to specific habitats and tasks, yet it is not known if bats also modify their calls to decrease atmospheric attenuation. Here the authors test the hypothesis that individuals emit echolocation calls ideally suited to current conditions of temperature and humidity. The authors recorded two species, Molossus molossus and Molossops temminckii, in the field under different conditions of humidity and temperature. For each species, two calls were analyzed: the shorter frequency modulated (FM) signals that bats emitted as they approached the recording microphone, and the longer constant frequency (CF) calls emitted thereafter. For each signal, the authors extracted peak frequency and duration, and compared these parameters among species, call type, and environmental conditions. The authors' results show significant differences in peak frequency and duration among environmental conditions for both call types. Bats decreased the frequency and increased duration of CF calls as atmospheric attenuation increased; using a lower-frequency call may increase the range of detection by a few meters as atmospheric attenuation increases. The same trend was not observed for FM calls, which may be explained by the primary role of these signals in short-range target localization.

Unveiling the Hidden Bat Diversity of a Neotropical Montane Forest.

Mountain environments, characterized by high levels of endemism, are at risk of experiencing significant biodiversity loss due to current trends in global warming. While many acknowledge their importance and vulnerability, these ecosystems still remain poorly studied, particularly for taxa that are difficult to sample such as bats. Aiming to estimate the amount of cryptic diversity among bats of a Neotropical montane cloud forest in Talamanca Range-south-east Central America-, we performed a 15-night sampling campaign, which resulted in 90 captured bats belonging to 8 species. We sequenced their mitochondrial cytochrome c oxidase subunit I (COI) and screened their inter- and intraspecific genetic variation. Phylogenetic relations with conspecifics and closely related species from other geographic regions were established using Maximum Likelihood and Bayesian inference methods, as well as median-joining haplotype networks. Mitochondrial lineages highly divergent from hitherto characterized populations (> 9% COI dissimilarity) were found in Myotis oxyotus and Hylonycteris underwoodi. Sturnira burtonlimi and M. keaysi also showed distinct mitochondrial structure with sibling species and/or populations. These results suggest that mountains in the region hold a high degree of endemicity potential that has previously been ignored in bats. They also warn of the high extinction risk montane bats may be facing due to climatic change, particularly in isolated mountain systems like Talamanca Range.

Repeatability in the contact calling system of Spix's disc-winged bat (Thyroptera tricolor).

Spix's disc-winged bat (Thyroptera tricolor) forms cohesive groups despite using an extremely ephemeral roost, partly due to the use of two acoustic signals that help individuals locate roost sites and group members. While the calls that aid in group cohesion are commonly used, some bats rarely or never produce them. Here, we examine whether the differences observed in the contact calling behaviour of T. tricolor are repeatable; that is, whether individual differences are consistent. We recorded contact calls of individuals in the field and rates and patterns of vocalization. To determine whether measured variables were consistent within individuals, we estimated repeatability (R), which compares within-individual to among-individual variance in behavioural traits. Our results show that repeatability for call variables was moderate but significant, and that repeatability was highest for the average number of calls produced (R=0.46-0.49). Our results demonstrate important individual differences in the contact calling behaviour of T. tricolor; we discuss how these could be the result of mechanisms such as frequency-dependent selection that favour groups composed of individuals with diverse vocal strategies. Future work should address whether changes in social environment, specifically group membership and social status, affect vocal behaviour.

Effects of roost specialization on extinction risk in bats.

Understanding causes and consequences of ecological specialization is of major concern in conservation. Specialist species are particularly vulnerable to human activities. If their food or habitats are depleted or lost, they may not be able to exploit alternative resources, and population losses may result. We examined International Union for Conservation of Nature (IUCN) Red List bat data and the number of roosts used per species (accounting for phylogenetic independence) to determine whether roost specialization is correlated with extinction risk. We found a significant correlation between the IUCN Red List category and the number of roost types used. Species that use fewer roost types had a higher risk of extinction. We found that caves and similar structures were the most widely used roost types, particularly by species under some level of risk of extinction. Many critically endangered, endangered, or vulnerable species used natural roosts exclusively, whereas less threatened species used natural and human-made roosts. Our results suggest that roost loss, particularly in species that rely on a single roost type, may be linked to extinction risk. Our focus on a single life history trait prevented us from determining how important this variable is for extinction risk relative to other variables, but we have taken a first step toward prioritizing conservation actions. Our results also suggest that roost specialization may exacerbate population declines due to other risk factors, such as hunting pressure or habitat loss, and thus that management actions to preserve species under risk of extinction should prioritize protection of roosting sites.

Sound amplification by means of a horn-like roosting structure in Spix's disc-winged bat.

While sound is a signal modality widely used by many animals, it is very susceptible to attenuation, hampering effective long-distance communication. A strategy to minimize sound attenuation that has been historically used by humans is to use acoustic horns; to date, no other animal is known to use a similar structure to increase sound intensity. Here, we describe how the use of a roosting structure that resembles an acoustic horn (the tapered tubes that form when new leaves of plants such as Heliconia or Calathea species start to unfurl) increases sound amplification of the incoming and outgoing social calls used by Spix's disc-winged bat (Thyroptera tricolor) to locate roosts and group members. Our results indicate that incoming calls are significantly amplified as a result of sound waves being increasingly compressed as they move into the narrow end of the leaf. Outgoing calls were faintly amplified, probably as a result of increased sound directionality. Both types of call, however, experienced significant sound distortion, which might explain the patterns of signal recognition previously observed in behavioural experiments. Our study provides the first evidence of the potential role that a roost can play in facilitating acoustic communication in bats.

Social calls produced within and near the roost in two species of tent-making bats, Dermanura watsoni and Ectophylla alba.

Social animals regularly face the problem of relocating conspecifics when separated. Communication is one of the most important mechanisms facilitating group formation and cohesion. Known as contact calls, signals exchanged between conspecifics that permit group maintenance are widespread across many taxa. Foliage-roosting bats are an excellent model system for studying the evolution of contact calling, as there are opportunities to compare closely related species that exhibit major differences in ecology and behavior. Further, foliage-roosting bats rely on relatively ephemeral roosts, which leads to major challenges in maintaining group cohesion. Here, we report findings on the communication signals produced by two tent-making bats, Dermanura watsoni and Ectophylla alba. We found that both species produced calls in the early morning near the roost that were associated with roostmate recruitment. Calling often ended once other bats arrived at the tent, suggesting that calls may be involved in roostmate recruitment and group formation. The structure and function of these calls are described and future research directions are discussed.

Response of a specialist bat to the loss of a critical resource.

Human activities have negatively impacted many species, particularly those with unique traits that restrict their use of resources and conditions to specific habitats. Unfortunately, few studies have been able to isolate the individual and combined effects of different threats on population persistence in a natural setting, since not all organisms can be associated with discrete habitat features occurring over limited spatial scales. We present the results of a field study that examines the short-term effects of roost loss in a specialist bat using a conspicuous, easily modified resource. We mimicked roost loss in the natural habitat and monitored individuals before and after the perturbation to determine patterns of resource use, spatial movements, and group stability. Our study focused on the disc-winged bat Thyroptera tricolor, a species highly morphologically specialized for roosting in the developing furled leaves of members of the order Zingiberales. We found that the number of species used for roosting increased, that home range size increased (before: mean 0.14±SD 0.08 ha; after: 0.73±0.68 ha), and that mean association indices decreased (before: 0.95±0.10; after: 0.77±0.18) once the roosting habitat was removed. These results demonstrate that the removal of roosting resources is associated with a decrease in roost-site preferences or selectivity, an increase in mobility of individuals, and a decrease in social cohesion. These responses may reduce fitness by potentially increasing energetic expenditure, predator exposure, and a decrease in cooperative interactions. Despite these potential risks, individuals never used roost-sites other than developing furled leaves, suggesting an extreme specialization that could ultimately jeopardize the long-term persistence of this species' local populations.

Social calls used by a leaf-roosting bat to signal location.

Social calls in bats have many functions, including mate attraction and maintaining contact during flight. Research suggests that social calls may also be used to transfer information about roosts, but no studies have yet demonstrated that calls are used to actively attract conspecifics to roosting locations. We document the social calls used by Spix's disc-winged bat (Thyroptera tricolor) to actively recruit group members to roosts. In acoustic trials, we recorded two sets of calls; one from flying individuals termed 'inquiry calls', and another from roosting bats termed 'response calls'. Inquiry calls were emitted by flying bats immediately upon release, and quickly (i.e. 178 ms) elicited production of response calls from roosting individuals. Most flying bats entered the roost when roosting individuals responded, while few bats entered the roost in the absence of a response. We argue that information transfer concerning roost location may facilitate sociality in T. tricolor, given the ephemeral nature of roosting structures used by this species.

Cooperative signaling behavior of roost location in a leaf-roosting bat.

Research suggests that social calls are important for conveying information about food and roost location in bats. However, no studies have specifically documented calls that are used to actively attract conspecifics to roosting locations. Here we describe the cooperative signaling behavior of roost location towards flying conspecifics in Spix's disc-winged bat (Thyroptera tricolor), a species that uses a highly ephemeral roosting resource. Two types of calls were recorded during field experiments; one from flying individuals termed "inquiry calls" and another from roosting bats termed "response calls". Inquiry calls were emitted by flying bats immediately upon release, and quickly elicited production of response calls from roosting individuals. Most flying bats entered the roost when roosting individuals responded, while very few bats entered the roost in the absence of a response. During playback experiments, we found significant differences in response rates among individuals, which could be caused by diverse intrinsic and extrinsic factors. In addition, results of our ongoing field studies suggest that the cooperative signaling behavior of roost location is important in maintaining social cohesion, and that the use of a larger home range when resources are scarcer may decrease group stability by hindering communication.