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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'.
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Quirópteros , Comportamento Social , Vocalização Animal , Quirópteros/fisiologia , Animais , Masculino , FemininoRESUMO
Social structure can emerge from hierarchically embedded scales of movement, where movement at one scale is constrained within a larger scale (e.g. among branches, trees, forests). In most studies of animal social networks, some scales of movement are not observed, and the relative importance of the observed scales of movement is unclear. Here, we asked: how does individual variation in movement, at multiple nested spatial scales, influence each individual's social connectedness? Using existing data from common vampire bats (Desmodus rotundus), we created an agent-based model of how three nested scales of movement-among roosts, clusters and grooming partners-each influence a bat's grooming network centrality. In each of 10 simulations, virtual bats lacking social and spatial preferences moved at each scale at empirically derived rates that were either fixed or individually variable and either independent or correlated across scales. We found that numbers of partners groomed per bat were driven more by within-roost movements than by roost switching, highlighting that co-roosting networks do not fully capture bat social structure. Simulations revealed how individual variation in movement at nested spatial scales can cause false discovery and misidentification of preferred social relationships. Our model provides several insights into how nonsocial factors shape social networks.
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Quirópteros , Comportamento Social , Animais , Quirópteros/fisiologia , Asseio Animal , MovimentoRESUMO
White-nose syndrome is a fungal disease that has decimated hibernating bats from multiple North American species. In 2014, the invasive fungus arrived at a hibernaculum of little brown bats (Myotis lucifugus) inside the spillway of Tippy Dam, located near Wellston, Michigan, USA, yet surprisingly, this population has not experienced the declines seen elsewhere. Unlike a typical subterranean hibernaculum, light enters the spillway through small ventilation holes. We hypothesized that this light causes the hibernating bats to maintain a circadian rhythm, thereby saving energy via social thermoregulation during synchronous arousals. To test this idea, we used high-resolution thermal cameras to monitor arousals from October 2019 to April 2020. We found that arousals followed a circadian rhythm, peaking after sunset, and that most observed arousals (>68%) occurred within a cluster of bats allowing for social thermoregulation. These findings are consistent with the hypothesis that light-induced synchronized arousals contribute to the unprecedented absence of mass mortality from white-nose syndrome in this large population. Using light to maintain a circadian rhythm in bats should be tested as a potential tool for mitigating mortality from white-nose syndrome. More generally, studying populations that have been largely unaffected by white-nose syndrome may provide insight into mitigation strategies for protecting the remaining populations.
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Quirópteros , Hibernação , Animais , Hibernação/fisiologia , Quirópteros/fisiologia , Regulação da Temperatura Corporal , Fungos , Nível de Alerta/fisiologiaRESUMO
Hemotropic mycoplasmas are emerging as a model system for studying bacterial pathogens in bats, but taxonomic coverage of sampled host species remains biased. We leveraged a long-term field study in Belize to uncover novel hemoplasma diversity in bats by analyzing 80 samples from 19 species, most of which are infrequently encountered. PCR targeting the partial 16S rRNA gene found 41% of bats positive for hemoplasmas. Phylogenetic analyses found two novel host shifts of hemoplasmas, four entirely new hemoplasma genotypes, and the first hemoplasma detections in four bat species. One of these novel hemoplasmas (from Neoeptesicus furinalis) shared 97.6% identity in the partial 16S rRNA gene to a human hemoplasma (Candidatus Mycoplasma haemohominis). Additional analysis of the partial 23S rRNA gene allowed us to also designate two novel hemoplasma species, in Myotis elegans and Phyllostomus discolor, with the proposed names Candidatus Mycoplasma haematomyotis sp. nov. and Candidatus Mycoplasma haematophyllostomi sp. nov., respectively. Our analyses show that additional hemoplasma diversity in bats can be uncovered by targeting rare or undersampled host species.
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Rabies virus (RABV) transmitted by the common vampire bat (Desmodus rotundus) poses a threat to agricultural development and public health throughout the Neotropics. The ecology and evolution of rabies host-pathogen dynamics are influenced by two infection-induced behavioural changes. RABV-infected hosts often exhibit increased aggression which facilitates transmission, and rabies also leads to reduced activity and paralysis prior to death. Although several studies document rabies-induced behavioural changes in rodents and other dead-end hosts, surprisingly few studies have measured these changes in vampire bats, the key natural reservoir throughout Latin America. Taking advantage of an experiment designed to test an oral rabies vaccine in captive male vampire bats, we quantify for the first time, to our knowledge, how rabies affects allogrooming and aggressive behaviours in this species. Compared to non-rabid vampire bats, rabid individuals reduced their allogrooming prior to death, but we did not detect increases in aggression among bats. To put our results in context, we review what is known and what remains unclear about behavioural changes of rabid vampire bats (resumen en español, electronic supplementary material, S1).
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Quirópteros , Vacina Antirrábica , Vírus da Raiva , Raiva , Animais , Masculino , Raiva/prevenção & controle , Raiva/veterináriaRESUMO
Permutation tests are widely used to test null hypotheses with animal social network data, but suffer from high rates of type I and II error when the permutations do not properly simulate the intended null hypothesis.Two common types of permutations each have limitations. Pre-network (or datastream) permutations can be used to control 'nuisance effects' like spatial, temporal or sampling biases, but only when the null hypothesis assumes random social structure. Node (or node-label) permutation tests can test null hypotheses that include nonrandom social structure, but only when nuisance effects do not shape the observed network.We demonstrate one possible solution addressing these limitations: using pre-network permutations to adjust the values for each node or edge before conducting a node permutation test. We conduct a range of simulations to estimate error rates caused by confounding effects of social or non-social structure in the raw data.Regressions on simulated datasets suggest that this 'double permutation' approach is less likely to produce elevated error rates relative to using only node permutations, pre-network permutations or node permutations with simple covariates, which all exhibit elevated type I errors under at least one set of simulated conditions. For example, in scenarios where type I error rates from pre-network permutation tests exceed 30%, the error rates from double permutation remain at 5%.The double permutation procedure provides one potential solution to issues arising from elevated type I and type II error rates when testing null hypotheses with social network data. We also discuss alternative approaches that can provide robust inference, including fitting mixed effects models, restricted node permutations, testing multiple null hypotheses and splitting large datasets to generate replicated networks. Finally, we highlight ways that uncertainty can be explicitly considered and carried through the analysis.
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Long-term memory has clear advantages for animals but also has neurological and behavioral costs1-3. Encoding memories is metabolically expensive1. Older memories can interfere with retrieval of more recent memories3, prolong decision-making and reduce cognitive flexibility2,3. Given these opposing selection pressures, understanding how long memories last can shed light on how memory enhances or constrains animals' abilities to exploit their niches. Although testing memory retention in wild animals is difficult, it is important because captive conditions do not reflect the complex cognitive demands of wild environments, and long-term captivity changes the brain4 (Data S1A). Here, we trained wild-caught frog-eating bats (Trachops cirrhosus) to find prey by flying to a novel acoustic cue. After they learned the rewarded sound, we released them back into the wild, and then re-captured some of them one to four years later. When re-tested, all eight 'experienced' bats that previously learned the novel prey sounds flew to those sounds within seconds, whereas 17 naïve bats tested with the same sounds showed weak responses. Experienced bats also showed behavior indicating generalization of memories between novel sounds and rewards over time. The frog-eating bat's remarkably long memory indicates that an ability to remember rarely encountered prey may be advantageous for this predator and suggests hitherto unknown cognitive abilities in bats.
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Quirópteros , Ecolocação , Animais , Anuros/fisiologia , Quirópteros/fisiologia , Ecolocação/fisiologia , Memória de Longo Prazo , Comportamento Predatório/fisiologia , SomRESUMO
Spatial assortment can be both a cause and a consequence of cooperation. Proximity promotes cooperation when individuals preferentially help nearby partners, and conversely, cooperation drives proximity when individuals move towards more cooperative partners. However, these two causal directions are difficult to distinguish with observational data. Here, we experimentally test if forcing randomly selected pairs of equally familiar female common vampire bats (Desmodus rotundus) into close spatial proximity promotes the formation of enduring cooperative relationships. Over 114 days, we sampled 682 h of interactions among 21 females captured from three distant sites to track daily allogrooming rates over time. We compared these rates before, during and after a one-week period, during which we caged random triads of previously unfamiliar and unrelated vampire bats in proximity. After the week of proximity when all bats could again freely associate, the allogrooming rates of pairs forced into proximity increased more than those of the 126 control pairs. This work is the first to experimentally demonstrate the causal effect of repeated interactions on cooperative investments in vampire bats. Future work should determine the relative importance of mere association versus interactions (e.g. reciprocal allogrooming) in shaping social preferences.
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Quirópteros , Animais , Feminino , HumanosRESUMO
Rapid advancements in biologging technology have led to unprecedented insights into animal behaviour, but testing the effects of biologgers on tagged animals is necessary for both scientific and ethical reasons. Here, we measured how quickly 13 wild-caught and captively isolated common vampire bats (Desmodus rotundus) habituated to mock proximity sensors glued to their dorsal fur. To assess habituation, we scored video-recorded behaviours every minute from 18.00 to 06.00 for 3 days, then compared the rates of grooming directed to the sensor tag versus to their own body. During the first hour, the mean tag-grooming rate declined dramatically from 53% of sampled time (95% CI = 36-65%, n = 6) to 16% (8-24%, n = 9), and down to 4% by hour 5 (1-6%, n = 13), while grooming of the bat's own body did not decline. When tags are firmly attached, isolated individual vampire bats mostly habituate within an hour of tag attachment. In two cases, however, tags became loose before falling off causing the bats to dishabituate. For tags glued to fur, behavioural data are likely to be impacted immediately after the tag is attached and when it is loose before it falls off.
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The 'social microbiome' can fundamentally shape the costs and benefits of group-living, but understanding social transmission of microbes in free-living animals is challenging due to confounding effects of kinship and shared environments (e.g. highly associated individuals often share the same spaces, food and water). Here, we report evidence for convergence towards a social microbiome among introduced common vampire bats, Desmodus rotundus, a highly social species in which adults feed only on blood, and engage in both mouth-to-body allogrooming and mouth-to-mouth regurgitated food sharing. Shotgun sequencing of samples from six zoos in the USA, 15 wild-caught bats from a colony in Belize and 31 bats from three colonies in Panama showed that faecal microbiomes were more similar within colonies than between colonies. To assess microbial transmission, we created an experimentally merged group of the Panama bats from the three distant sites by housing these bats together for four months. In this merged colony, we found evidence that dyadic gut microbiome similarity increased with both clustering and oral contact, leading to microbiome convergence among introduced bats. Our findings demonstrate that social interactions shape microbiome similarity even when controlling for past social history, kinship, environment and diet.
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Quirópteros , Microbioma Gastrointestinal , Animais , Fezes , Alimentos , HumanosRESUMO
Stable social bonds in group-living animals can provide greater access to food. A striking example is that female vampire bats often regurgitate blood to socially bonded kin and nonkin that failed in their nightly hunt. Food-sharing relationships form via preferred associations and social grooming within roosts. However, it remains unclear whether these cooperative relationships extend beyond the roost. To evaluate if long-term cooperative relationships in vampire bats play a role in foraging, we tested if foraging encounters measured by proximity sensors could be explained by wild roosting proximity, kinship, or rates of co-feeding, social grooming, and food sharing during 21 months in captivity. We assessed evidence for 6 hypothetical scenarios of social foraging, ranging from individual to collective hunting. We found that closely bonded female vampire bats departed their roost separately, but often reunited far outside the roost. Repeating foraging encounters were predicted by within-roost association and histories of cooperation in captivity, even when accounting for kinship. Foraging bats demonstrated both affiliative and competitive interactions with different social calls linked to each interaction type. We suggest that social foraging could have implications for social evolution if "local" within-roost cooperation and "global" outside-roost competition enhances fitness interdependence between frequent roostmates.
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Comportamento Apetitivo , Quirópteros/fisiologia , Comportamento Cooperativo , Animais , Bovinos , Comportamento Alimentar , Feminino , Comportamento Social , Vocalização AnimalRESUMO
When group-living animals develop individualized social relationships, they often regulate cooperation and conflict through a dominance hierarchy. Female common vampire bats have been an experimental system for studying cooperative relationships, yet surprisingly little is known about female conflict. Here, we recorded the outcomes of 1023 competitive interactions over food provided ad libitum in a captive colony of 33 vampire bats (24 adult females and their young). We found a weakly linear dominance hierarchy using three common metrics (Landau's h' measure of linearity, triangle transitivity and directional consistency). However, patterns of female dominance were less structured than in many other group-living mammals. Female social rank was not clearly predicted by body size, age, nor reproductive status, and competitive interactions were not correlated with kinship, grooming nor food sharing. We therefore found no evidence that females groomed or shared food up a hierarchy or that differences in rank explained asymmetries in grooming or food sharing. A possible explanation for such apparently egalitarian relationships among female vampire bats is the scale of competition. Female vampire bats that are frequent roostmates might not often directly compete for food in the wild.
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Individual animals across many different species occasionally 'adopt' unrelated, orphaned offspring. Although adoption may be best explained as a by-product of adaptive traits that enhance parental care or promote the development of parental skills, one factor that is possibly important for the likelihood of adoption is the history of cooperative interactions between the mother, adopted offspring and adopter. Using 652 h of behavioural samples collected over four months, we describe patterns of allogrooming and food sharing before and after an instance of non-kin adoption between two adult female common vampire bats (Desmodus rotundus) that were captured from distant sites (340 km apart) and introduced to one another in captivity. The first female died from an illness 19 days after giving birth. The second female groomed and regurgitated food to the mother more often than any other group member, then groomed, nursed and regurgitated food to the orphaned, female pup. The substantial increase in alloparental care by this female after the mother's death was not observed among the 20 other adult females that were present in the colony. Our findings corroborate previous reports of non-kin adoption in common vampire bats and are consistent with the hypothesis that non-kin adoption can be motivated, in part, by a history of cooperative interactions.
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Exceptionally long-lived species, including many bats, rarely show overt signs of aging, making it difficult to determine why species differ in lifespan. Here, we use DNA methylation (DNAm) profiles from 712 known-age bats, representing 26 species, to identify epigenetic changes associated with age and longevity. We demonstrate that DNAm accurately predicts chronological age. Across species, longevity is negatively associated with the rate of DNAm change at age-associated sites. Furthermore, analysis of several bat genomes reveals that hypermethylated age- and longevity-associated sites are disproportionately located in promoter regions of key transcription factors (TF) and enriched for histone and chromatin features associated with transcriptional regulation. Predicted TF binding site motifs and enrichment analyses indicate that age-related methylation change is influenced by developmental processes, while longevity-related DNAm change is associated with innate immunity or tumorigenesis genes, suggesting that bat longevity results from augmented immune response and cancer suppression.
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Quirópteros/genética , Metilação de DNA , Longevidade/genética , Envelhecimento/genética , Animais , Carcinogênese/genética , Cromatina , Epigênese Genética , Técnicas Genéticas , Histonas , Imunidade Inata/genética , FilogeniaRESUMO
The social decisions that individuals make-who to interact with and how frequently-give rise to social structure. The resulting social structure then determines how individuals interact with their surroundings-resources and risks, pathogens and predators, competitors and cooperators. However, despite intensive research on (a) how individuals make social decisions and (b) how social structure shapes social processes (e.g. cooperation, competition and conflict), there are still few studies linking these two perspectives. These perspectives represent two halves of a feedback loop: individual behaviour scales up to define the social environment, and this environment, in turn, feeds back by shaping the selective agents that drive individual behaviour. We first review well-established research areas that have captured both elements of this feedback loop-host-pathogen dynamics and cultural transmission. We then highlight areas where social structure is well studied but the two perspectives remain largely disconnected. Finally, we synthesise existing research on 14 distinct research topics to identify new prospects where the interplay between social structure and social processes are likely to be important but remain largely unexplored. Our review shows that the inherent links between individuals' traits, their social decisions, social structure and social evolution, warrant more consideration. By mapping the existing and missing connections among many research areas, our review highlights where explicitly considering social structure and the individual-to-society feedbacks can reveal new dimensions to old questions in ecology and evolution.
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Evolução Biológica , Comportamento Social , Animais , Ecologia , Retroalimentação , Meio SocialRESUMO
Many animals use social cues to find refuges. Bats can find roosts using the echolocation and social calls of conspecifics, but they might also use scent cues, a possibility which is less studied. The entrances of bat roosts are often marked by guano and urine, providing possible scent cues. We conducted eight experiments to test whether bats use the scent of guano and urine to find potential roosts. In field experiments, we tested if Molossus molossus (velvety free-tailed bats) in Panama and Eptesicus fuscus (big brown bats) in Ohio would investigate artificial roost boxes that were scented with guano and urine more often than a paired unscented control. We did not detect any difference in flights near the scented versus unscented roosts, and we detected only one entrance into any artificial roost (scented). In six captive experiments, we tested for the attraction of Desmodus rotundus (common vampire bats) and Molossus molossus to areas scented with guano and urine, under several conditions. Results were mixed, but overall suggested that the scent of guano and urine does not act as a strong lure for the tested bat species. We suggest that further tests of olfaction-based roost choice in bats should manipulate existing scent cues on familiar roosts.
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Vocalizations are an important means to facilitate social interactions, but vocal communication may be affected by infections. While such effects have been shown for mate-attraction calls, other vocalizations that facilitate social contact have received less attention. When isolated, vampire bats produce contact calls that attract highly associated groupmates. Here, we test the effect of an immune challenge on contact calling rates of individually isolated vampire bats. Sickness behaviour did not appear to change call structure, but it decreased the number of contact calls produced. This effect could decrease contact with groupmates and augment other established mechanisms by which sickness reduces social encounters (e.g. mortality, lethargy and social withdrawal or disinterest).