Biology subjects

Carter, G. G.

Publications and source records attributed to Carter, G. G..

17 recordsLinked to original sources

bioRxiv2026

Socially transmitted knowledge of hibernation sites in bats

In temperate regions around the world, bats travel long distances every winter to gather at hibernation sites. A longstanding hypothesis is that each new generation of bats learns about the locations of these sites (called hibernacula) from older individuals, yet clear and compelling evidence demonstrating social transmission of this knowledge has been lacking. Here, we compiled 30,882 observations from 1985 to 2023 of 13,852 Greater mouse-eared bats (Myotis myotis) that were banded and observed at summer roosts, winter hibernacula, or both. Our analyses revealed four lines of evidence that Greater mouse-eared bats find suitable hibernacula using social information acquired at summer roosts. First, naive yearlings were more likely to be seen sharing their first hibernacula with adults from their summer birth colony relative to a null model where bats moved independently. Second, adult bats were also more likely to co-switch together into the same hibernacula across winters than expected from independent movements. Third, bats that roosted together in the summer were more likely to share a different site as a hibernaculum during the winter: being observed together during a summer changed the probability of a pair being observed together during a winter from 5% to 12%. Finally, high-resolution tracking revealed an instance of tandem flights to hibernacula sites during the summer, demonstrating that yearlings can learn from experienced adult bats months before hibernation. Together, our findings show that maternity colonies serve as "information centers" where females acquire knowledge of suitable hibernation sites throughout their long lives.

animal behavior and cognition↗

bioRxiv2026

Cross-Continental Analysis of Vampire Bat Betaherpesvirus Reveals Limited Interference Among Strains and Local Geographic Spread

Desmodus rotundus Betaherpesvirus (DrBHV) is a candidate vector for a transmissible vaccine targeting the circulation of rabies virus within its vampire bat reservoir. Studies assessing the potential for DrBHV as a vector have not considered its geographic range, potential for transboundary spread or how the diversity of wildtype DrBHV in natural bat populations might impede the spread of a modified vaccine strain. Here, by sequencing DrBHVs from vampire bats spanning 15 regions across 7 rabies-affected countries in Latin America and the Caribbean, we characterise the continent-scale distribution of DrBHV diversity and demonstrate widespread and apparently unconstrained co-infection. DrBHV occurred in all regions, forming a monophyletic clade consistent with a single introduction to vampire bats or host-virus co-speciation rather than frequent host switching. Phylogeographic analyses revealed cross-boundary spread that was predicted by geographic proximity. We identified 50 putative DrBHV strains and 79% of DrBHV-infected bats harboured multiple strains. No strains were over- or under-represented in co-infection and co-infections occurred proportionately to local strain prevalence. Whether strains circulated in given populations was predominantly driven by the geographic proximity of other populations containing that strain. The evolutionary relatedness of strains constrained neither rates of co-infection within individuals nor whether strains co-circulated within regions, suggesting vaccine vectors might be locally sourced rather than requiring imported, divergent strains to ameliorate interference. These results support the viability of DrBHV-vectored vaccines for mitigating rabies virus across Latin America and the Caribbean, despite widespread circulation of wildtype viruses.

genomics↗

bioRxiv2026

Contact calling is predicted by cooperative relationships in vampire bats

Group-living animals often coordinate their behavior using "contact calls". Identifying the function of these calls requires testing whether they are intended for any group member or targeted to specific preferred associates. If contact calling is used to coordinate with preferred associates, then higher rates of contact calling are expected between group members with a history of more frequent affiliation and cooperation. To test this hypothesis, we constructed a contact-calling network using synchronized recordings of vocal interactions between all 28 possible pairs of 8 female common vampire bats with well-sampled histories of social grooming and regurgitated food sharing. Bayesian multilevel models show that pairwise rates of contact calling were clearly predicted by social grooming and cooperative allofeeding rates in ways not explained by kinship. These findings show that common vampire bats use contact calls to coordinate with specific same-sex associates, unlike other studied bat species where individuals produce contact calls at similar rates towards different group members. We also found that, compared to white-winged vampire bats, common vampire bats are ten times less likely to rapidly respond to a contact call; this suggests yet-to-be-discovered differences in social behavior between vampire bat species. Finally, we discuss implications for the vocal grooming hypothesis.

animal behavior and cognition↗

bioRxiv2026

Vampire bats target their social grooming to hard-to-reach body parts

Many group-living mammals and birds groom the fur (or preen the feathers) of their close associates to build and maintain affiliative relationships. Several lines of evidence suggest that social grooming in female common vampire bats (Desmodus rotundus) is a low-cost form of helping, but it has yet to be shown that vampire bats preferentially groom others in locations that are difficult to self-groom, as has been found in multiple primate species. In this short note, we show that vampire bat social grooming (n = 1586 events) occurs most often on parts of the recipient's body where self-grooming (n = 1515 events) is least likely, and often in locations where the recipient could not lick itself, like the back of the head. The finding that vampire bats preferentially groom each other in hard-to-reach locations provides further support for the hypothesis that social grooming is both a social signal and a low-cost form of helping.

animal behavior and cognition↗

bioRxiv2025

Vocal convergence during formation of social relationships in vampire bats

In many group-living birds and mammals, the formation of affiliative relationships is hypothesized to cause vocal convergence (an increase in call similarity between individuals). However, testing this causal effect can be difficult, because it requires experimentally forming new relationships. Here, we demonstrate convergence in the contact calls of common vampire bats (Desmodus rotundus) that we introduced and experimentally housed together. To estimate and disentangle the roles of kinship, co-housing (familiarity), allogrooming, and food sharing in predicting call similarity, we first measured call similarity using 35 features of 693,494 contact calls from 95 bats, then fit a series of Bayesian generalized multi-membership models. We also measured changes in call similarity for a subset of individuals that were recorded before and after co-housing. We found that co-housing caused vocal convergence. Furthermore, food-sharing rates among familiar nonkin within the same co-housed group predicted contact call similarity. This finding suggests that the development of cooperative relationships causes further vocal convergence beyond the initial convergence caused by co-housing. Our findings have implications for the development of cooperative relationships and vocal learning.

animal behavior and cognition↗

bioRxiv2022

Social effects of rabies infection in male vampire bats (Desmodus rotundus)

Abstract (resumen en espanol, S1)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 behavioral 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 behavioral 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. Here, we take advantage of an experiment designed to test the safety and efficacy of an oral rabies vaccine in captive male vampire bats to quantify for the first time how rabies affects allogrooming and aggressive behaviors in the vampire bat. 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 behavioral changes of rabid vampire bats.

animal behavior and cognition↗

bioRxiv2022

Spatial learning overshadows learning novel odors and sounds in both a predatory and a frugivorous bat

AO_SCPLOWBSTRACTC_SCPLOWTo be efficient while foraging, animals should be selective about attending to and remembering 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 and feature cues. Animals that store food or feed on spatially stable food, like fruit or flowers, should be predisposed to learning a meals location, whereas predators that hunt mobile prey should instead be biased towards learning feature cues such as color or sound. Previous studies suggest that nectar- and fruit-feeding bats should rely relatively more on spatial cues, whereas predatory bats should 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 odor, sound, and location. We then dissociated these cues to assess which cue each bat had learned. Rather than finding that the frugivore and predator are on opposite ends of a continuum in their relative reliance on spatial and feature cues, we found that both species learned spatial cues with no evidence that either learned the sounds or odors. We discuss interpretations of these results in the context of past work on use of spatial cues versus feature cues. Compared to feature cues, spatial cues may be fundamentally more rich, salient, or memorable. LO_SCPLOWAYC_SCPLOW SO_SCPLOWUMMARYC_SCPLOWWhen animals learn how to obtain food, they could attend to many possible cues--such as the associated smells, sights, sounds, or locations of the food. It has been hypothesized that natural selection has shaped animals to pay particular attention to the types of cues that are most useful for finding their typical food. In bats, this would predict that predatory species that hunt mobile, noisy insects by sound should be biased towards learning a food-associated sound, whereas bats that eat stationary and silent fruit should be biased towards learning a foods location. We gave predatory and fruit-eating bats the opportunity to simultaneously learn food-rewarded odors, sounds, or locations. Regardless of their diets, both species of bats learned locations rather than the odors or sounds associated with food. Spatial cues may be particularly rich or salient, and when they are reliable, animals may use them for learning over other cues regardless of their typical food.

animal behavior and cognition↗

bioRxiv2022

Long-term memory in frog-eating bats

Long-term memory has clear advantages but also has neurological and behavioral costs1-3. 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 (past studies on nonhuman long-term memory are reviewed in Table S1). Here, we trained wild-caught frog-eating bats (Trachops cirrhosus) to find prey by flying to a novel acoustic cue, released them back into the wild, and then re-captured some of them 1-4 years later. When re-tested, all eight experienced bats that previously learned the novel prey sounds flew to those sounds within seconds, whereas 17 naive 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 bats remarkably long memory for novel acoustic cues indicates that an ability to remember rarely encountered prey may be advantageous for this predator, and suggests hitherto unknown cognitive abilities in bats. O_TBL View this table: org.highwire.dtl.DTLVardef@15a8294org.highwire.dtl.DTLVardef@132eb3forg.highwire.dtl.DTLVardef@1f29583org.highwire.dtl.DTLVardef@135dff2org.highwire.dtl.DTLVardef@19cfa_HPS_FORMAT_FIGEXP M_TBL O_FLOATNOTable S1:C_FLOATNO O_TABLECAPTIONStudies of animal memory durations documenting memories of months or years. Memory duration = the longest duration demonstrated in the study. Wild or captive = where animals spent the time of memory retention; some "captive" animals were originally wild caught. Context = the ecological context and memory task being tested. 2-AFC = Two-alternative forced choice. C_TABLECAPTION C_TBL

animal behavior and cognition↗

bioRxiv2022

Forced proximity promotes the formation of enduring cooperative relationships in vampire bats

Spatial assortment can be both a cause and 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 hours 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 close proximity. After the week of close 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.

animal behavior and cognition↗

bioRxiv2021

Social foraging in vampire bats is predicted by long-term cooperative relationships

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 22 months in captivity. We assessed evidence for six hypothetical scenarios of social foraging, ranging from individual to collective hunting. We found that female vampire bats departed their roost individually, but often re-united far outside the roost. Nonrandomly repeating foraging encounters were predicted by within-roost association and histories of cooperation in captivity, even when controlling for kinship. Foraging bats demonstrated both affiliative and competitive interactions and a previously undescribed call type. We suggest that social foraging could have implications for social evolution if local cooperation within the roost and global competition outside the roost enhances fitness interdependence between frequent roostmates.

animal behavior and cognition↗

bioRxiv2020

Genome Methylation Predicts Age and Longevity of Bats

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.

genomics↗

bioRxiv2020

Permutation tests for hypothesis testing with animal social data: problems and potential solutions

O_LIPermutation 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. C_LIO_LITwo 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. C_LIO_LIWe 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. C_LIO_LIRegressions 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%. C_LIO_LIThe 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. C_LI

animal behavior and cognition↗

bioRxiv2020

Immune-challenged vampire bats produce fewer contact calls

Infections can affect how animals vocalize and, hence, interact with conspecifics. While this effect has been shown for mate-attraction calls, other vocalizations that facilitate social contact have received less attention. When isolated, vampire bats produce contact calls which attract highly associated groupmates. Here, we test the effect of an immune challenge on contact calling rates of individually isolated vampire bats. Sickness behavior 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).

animal behavior and cognition↗

bioRxiv2020

Sickness behaviour reduces network centrality in wild vampire bats

Sickness behaviours, like lethargy, can slow the spread of pathogens across a social network. We conducted a field experiment to investigate how sickness behaviour reduces individual connectedness in a high-resolution dynamic social network. We captured adult female vampire bats (Desmodus rotundus) from a wild roost. To create sick bats, we injected a random half of the bats (n=16) with the immune-challenging substance, lipopolysaccharide, and injected control bats with saline (n=15). Over the next three days, we used proximity sensors to continuously track their associations under natural conditions. The sick bats showed a clear decrease in social connectedness (degree, strength, and eigenvector centrality). Bats in the control group encountered fewer sick bats and also spent less time near them. These effects varied by time of day and declined over 48 hours. High-resolution proximity data allow researchers to define network connections based on how a pathogen spreads (e.g. the minimum contact time or distance for transmission). We therefore show how the estimate of the sickness effect changes as network ties are defined using varying distances and durations of association. Tracking the effects of sickness behaviour on high-resolution dynamic social networks can help create more sophisticated simulations of pathogen transmission through structured populations.

animal behavior and cognition↗

bioRxiv2019

Evidence for unfamiliar kin recognition in vampire bats

Kin discrimination allows organisms to preferentially cooperate with kin, reduce kin competition, and avoid inbreeding. In vertebrates, kin discrimination often occurs through prior association. There is less evidence for recognition of unfamiliar kin. Here, we present the first evidence of unfamiliar kin recognition in bats. We captured female vampire bats (Desmodus rotundus) from a single roost, allowed them to breed in captivity for 22 months, then released 17 wild-caught females and six captive-born daughters back into the same wild roost. We then used custom-built proximity sensors to track the free-ranging social encounters among the previously captive bats and 27 tagged control bats from the same roost. Using microsatellite-based relatedness estimates, we found that previously captive bats preferentially associated with related control bats, and that captive-born bats preferentially associated with unfamiliar kin among control bats. Closer analyses showed that these unfamiliar-kin-biased associations were not caused by mothers or other familiar close kin, because the kinship bias was evident even when those bats were not nearby. This striking evidence for unfamiliar kin recognition in vampire bats warrants further investigation and provides new hypotheses for how cooperative relationships might be driven synergistically by both social experience and phenotypic similarity.

animal behavior and cognition↗

bioRxiv2019

Thinking small: next-generation sensor networks close the size gap in vertebrate biologging

Recent advances in animal tracking technology have ushered in a new era in biologging. However, the considerable size of many sophisticated biologging devices restricts their application to larger animals, while old-fashioned techniques often still represent the state-of-the-art for studying small vertebrates. In industrial applications, low-power wireless sensor networks fulfill requirements similar to those needed to monitor animal behavior at high resolution and at low tag weight. We developed a wireless biologging network (WBN), which enables simultaneous direct proximity sensing, high-resolution tracking, and long-range remote data download at tag weights of one to two grams. Deployments to study wild bats created social networks and flight trajectories of unprecedented quality. Our developments highlight the vast capabilities of WBNs and their potential to close an important gap in biologging: fully automated tracking and proximity sensing of small animals, even in closed habitats, at high spatial and temporal resolution.

animal behavior and cognition↗

bioRxiv2019

Development of new food-sharing relationships among nonkin vampire bats

In an individualized animal society, social bonds can foster cooperation and enhance survival and reproduction. Cooperative bonds often exist among kin, but nonkin can also develop high-investment cooperative bonds that share similarities with human friendship. How do such bonds form? One theory suggests that strangers should test the waters of a new relationship by making small initial cooperative investments and gradually escalating them with good partners. This raising-the-stakes strategy is demonstrated by human strangers in short-term economic games, but it remains unclear whether it applies to helping in a natural long-term social bond. Here we show evidence that unfamiliar vampire bats (Desmodus rotundus) selectively escalate low-cost investments in allogrooming before developing higher-cost food-sharing relationships. We introduced females from geographically distant sites in pairs or groups and observed that bats established new reciprocal grooming relationships, and that increasing grooming rates predicted the occurrence of first food donations, at which point grooming rates no longer increased. New food-sharing relationships emerged reciprocally in 14% of female pairs, typically over 10-15 months, and developed faster when strangers lacked alternative familiar partners. A gradual grooming-to-sharing transition among past strangers suggests that raising the stakes might be more evident when tracking multiple cooperative behaviours as new relationships form, rather than measuring a single behavior in an established relationship. Raising the stakes could play a similar underappreciated role across a broader spectrum of social decisions with long-term consequences, such as joining a new social group or forming a long-term pair-bond. Significance statementVampire bats form long-term cooperative social bonds that involve reciprocal food sharing. How do two unrelated bats go from being strangers to having a high-investment food-sharing relationship? We introduced unfamiliar bats and found evidence that low-cost grooming paves the way for higher-cost food donations. Food sharing emerged in a reciprocal fashion and it emerged faster when two strangers did not have access to their original groupmates. The bats that formed new food-sharing relationships had a history of escalating reciprocal grooming up until the food sharing began. Our finding that unfamiliar nonkin vampire bats appear to gradually and selectively transition from low-cost to high-cost cooperative behaviors is the first evidence that nonhuman individuals raise the stakes when forming new cooperative relationships.

animal behavior and cognition↗