Secretions of the interaural gland contain information about individuality and colony membership in the Bechstein's bat

Mammals use chemical signals for individual and kin recognition, to establish social hierarchies, mark territories and choose mates. The nocturnal and social lifestyle of bats suggests that, besides acoustic signals, they also use scent to communicate. We investigated in the communally breeding Bechstein's bat, Myotis bechsteinii, whether secretions of the facial interaural gland contain information that can be used for individual and colony recognition. Since female Bechstein's bats live in closed societies and show cooperative behaviour, we predicted they would recognize colony members. We analysed interaural gland secretions, which we repeatedly sampled from 85 females belonging to four free-ranging colonies. Gas chromatography/mass spectrometry profiles were individually specific and differed between colonies. Comparing odour profiles between colonies we found a relation between chemical similarity and the mitochondrial haplotype of colony members. Within colonies there was no correlation between mass spectrometer profile similarity and genetic relatedness. Our results suggest that female Bechstein's bats may use interaural gland secretions for individual and colony recognition but not to infer kinship directly.Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

‘Compromise’ in Echolocation Calls between Different Colonies of the Intermediate Leaf-Nosed Bat (Hipposideros larvatus)

Each animal population has its own acoustic signature which facilitates identification, communication and reproduction. The sonar signals of bats can convey social information, such as species identity and contextual information. The goal of this study was to determine whether bats adjust their echolocation call structures to mutually recognize and communicate when they encounter the bats from different colonies. We used the intermediate leaf-nosed bats (Hipposideros larvatus) as a case study to investigate the variations of echolocation calls when bats from one colony were introduced singly into the home cage of a new colony or two bats from different colonies were cohabitated together for one month. Our experiments showed that the single bat individual altered its peak frequency of echolocation calls to approach the call of new colony members and two bats from different colonies adjusted their call frequencies toward each other to a similar frequency after being chronically cohabitated. These results indicate that the ‘compromise’ in echolocation calls might be used to ensure effective mutual communication among bats.     

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 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.

A combination of captive experiments and proximity sensing in the wild show that social bonds in vampire bats that are typically defined by cooperative interactions within the roost also extend beyond the roost and may provide benefits during foraging.     

Group Hunting—A Reason for Sociality in Molossid Bats?

Many bat species live in groups, some of them in highly complex social systems, but the reasons for sociality in bats remain largely unresolved. Increased foraging efficiency through passive information transfer in species foraging for ephemeral insects has been postulated as a reason for group formation of male bats in the temperate zones. We hypothesized that benefits from group hunting might also entice tropical bats of both sexes to live in groups. Here we investigate whether Molossus molossus, a small insectivorous bat in Panama, hunts in groups. We use a phased antenna array setup to reduce error in telemetry bearings. Our results confirmed that simultaneously radiotracked individuals from the same colony foraged together significantly more than expected by chance. Our data are consistent with the hypothesis that many bats are social because of information transfer between foraging group members. We suggest this reason for sociality to be more widespread than currently assumed. Furthermore, benefits from group hunting may also have contributed to the evolution of group living in other animals specialized on ephemeral food sources.     

Relatedness,parentage, and philopatry within a Natterer’s bat (<Emphasis Type="Italic">Myotis nattereri</Emphasis>) maternity colony

Given their cryptic behaviour, it is often difficult to establish kinship within microchiropteran maternity colonies. This limits understanding of group formation within this highly social group. Following a concerted effort to comprehensively sample a Natterer’s bat (Myotis nattereri) maternity colony over two consecutive summers, we employed microsatellite DNA profiling to examine genetic relatedness among individuals. Resulting data were used to ascertain female kinship, parentage, mating strategies, and philopatry. Overall, despite evidence of female philopatry, relatedness was low both for adult females and juveniles of both sexes. The majority of individuals within the colony were found to be unrelated or distantly related. However, parentage analysis indicates the existence of a number of maternal lineages (e.g., grandmother, mother, or daughter). There was no evidence suggesting that males born within the colony are mating with females of the same colony. Thus, in this species, males appear to be the dispersive sex. In the Natterer’s bat, colony formation is likely to be based on the benefits of group living, rather than kin selection.     

Abdominal microbial communities in ants depend on colony membership rather than caste and are linked to colony productivity

Gut bacteria aid their host in digestion and pathogen defense, and bacterial communities that differ in diversity or composition may vary in their ability to do so. Typically, the gut microbiomes of animals living in social groups converge as members share a nest environment and frequently interact. Social insect colonies, however, consist of individuals that differ in age, physiology, and behavior, traits that could affect gut communities or that expose the host to different bacteria, potentially leading to variation in the gut microbiome within colonies. Here we asked whether bacterial communities in the abdomen of Temnothorax nylanderi ants, composed largely of the gut microbiome, differ between different reproductive and behavioral castes. We compared microbiomes of queens, newly eclosed workers, brood carers, and foragers by high‐throughput 16S rRNA sequencing. Additionally, we sampled individuals from the same colonies twice, in the field and after 2 months of laboratory housing. To disentangle the effects of laboratory environment and season on microbial communities, additional colonies were collected at the same location after 2 months. There were no large differences between ant castes, although queens harbored more diverse microbial communities than workers. Instead, we found effects of colony, environment, and season on the abdominal microbiome. Interestingly, colonies with more diverse communities had produced more brood. Moreover, the queens' microbiome composition was linked to egg production. Although long‐term coevolution between social insects and gut bacteria has been repeatedly evidenced, our study is the first to find associations between abdominal microbiome characteristics and colony productivity in social insects.     

Long-Term Disease Dynamics for a Specialized Parasite of Ant Societies: A Field Study

Many studies have investigated how social insects behave when a parasite is introduced into their colonies. These studies have been conducted in the laboratory, and we still have a limited understanding of the dynamics of ant-parasite interactions under natural conditions. Here we consider a specialized parasite of ant societies (Ophiocordyceps camponoti-rufipedis infecting Camponotus rufipes) within a rainforest. We first established that the parasite is unable to develop to transmission stage when introduced within the host nest. Secondly, we surveyed all colonies in the studied area and recorded 100% prevalence at the colony level (all colonies were infected). Finally, we conducted a long-term detailed census of parasite pressure, by mapping the position of infected dead ants and foraging trails (future hosts) in the immediate vicinity of the colonies over 20 months. We report new dead infected ants for all the months we conducted the census – at an average of 14.5 cadavers/month/colony. Based on the low infection rate, the absence of colony collapse or complete recovery of the colonies, we suggest that this parasite represents a chronic infection in the ant societies. We also proposed a “terminal host model of transmission” that links the age-related polyethism to the persistence of a parasitic infection.     

Analyzing NEXRAD doppler radar images to assess nightly dispersal patterns and population trends in Brazilian free-tailed bats (Tadarida brasiliensis)

Operators of early weather-surveillance radars often observedechoes on their displays that did not behave like weather pattern,including expanding ring-like shapes they called angels. Theseechoes were caused by high-flying insects, migrating birds,and large colonies of bats emerging from roosts to feed. Modernweather-surveillance radar stations in the United States (NEXt-generationRADar or NEXRAD) provide detailed images that clearly show eveningbat emergences from large colonies. These images can be usedto investigate the flight behavior of groups of bats and populationtrends in large colonies of Brazilian free-tailed bats (Tadaridabrasiliensis) in south-central Texas which are clearly imagedby local NEXRAD radar stations. In this study, we used radarreflectivity data from the New Braunfels, Texas NEXRAD stationto examine relative colony size, direction of movement, speedof dispersion, and altitude gradients of bats from these coloniesfollowing evening emergence. Base reflectivity clear-air-modeLevel-II images were geo-referenced and compiled in a GIS alongwith locations of colonies and features on the landscape. Temporalsequences of images were filtered for the activity of bats,and from this, the relative size of bat colonies, and the speedand heading of bat emergences were calculated. Our results indicatecyclical changes in colony size from year to year and that initialheadings taken by bats during emergence flights are highly directional.We found that NEXRAD data can be an effective tool for monitoringthe nightly behavior and seasonal changes in these large colonies.Understanding the distribution of a large regional bat populationon a landscape scale has important implications for agriculturalpest management and conservation efforts.     

Female Bechstein's Bats Share Foraging Sites with Maternal Kin but do not Forage Together with them – Results from a Long‐Term Study

In many social animals, group members exchange information about where to feed. Thereby, they may gain direct benefits, for example, if social hunting enhances individual foraging success. Alternatively, individuals may receive indirect fitness benefits by preferentially sharing information about suitable feeding sites with kin. Indeed, in some species, a positive correlation between the degree of relatedness among individuals and the overlap among their foraging areas was found. However, sharing foraging sites with kin can also have costs if it increases food competition, which is not compensated by direct benefits. The goal of this study was to investigate whether sharing of individual foraging areas in female Bechstein's bats is best explained by kin selection or by direct benefits through social foraging. To assess their individual foraging behaviour, we analysed radio‐tracking data of 22 members of one maternity colony, including nine mother–daughter pairs, seven pairs of less closely related individuals and six pairs of unrelated bats. We examined the bats' fidelity to specific foraging areas during several years and quantified the influence of kinship on the overlap among individual foraging areas. By measuring how close to each other the bats foraged, we assessed whether individuals with overlapping areas are likely to forage together. Our study confirms previous findings that Bechstein's bats show high fidelity to foraging areas across years. Moreover, we found that relatives share foraging areas significantly more often compared with unrelated colony members. Finally, our data reveal for the first time that most colony members that share foraging areas are unlikely to forage together. This suggests that female Bechstein's bats gain no direct benefits from sharing foraging areas with members of the same maternal lineage. Our findings also have implications for conservation as habitat loss within a colony's home range might expose entire matrilines to high risks.     

Spatio-temporal population genetic structure of the parasitic mite Spinturnix bechsteini is shaped by its own demography and the social system of its bat host

Information about the population genetic structures of parasites is important for an understanding of parasite transmission pathways and ultimately the co-evolution with their hosts. If parasites cannot disperse independently of their hosts, a parasite's population structure will depend upon the host's spatial distribution. Geographical barriers affecting host dispersal can therefore lead to structured parasite populations. However, how the host's social system affects the genetic structure of parasite populations is largely unknown. We used mitochondrial DNA (mtDNA) to describe the spatio-temporal population structure of a contact-transmitted parasitic wing mite ( Spinturnix bechsteini ) and compared it to that of its social host, the Bechstein's bat ( Myotis bechsteinii ). We observed no genetic differentiation between mites living on different bats within a colony. This suggests that mites can move freely among bats of the same colony. As expected in case of restricted inter-colony dispersal, we observed a strong genetic differentiation of mites among demographically isolated bat colonies. In contrast, we found a strong genetic turnover between years when we investigated the temporal variation of mite haplotypes within colonies. This can be explained with mite dispersal occuring between colonies and bottlenecks of mite populations within colonies. The observed absence of isolation by distance could be the result from genetic drift and/or from mites dispersing even between remote bat colonies, whose members may meet at mating sites in autumn or in hibernacula in winter. Our data show that the population structure of this parasitic wing mite is influenced by its own demography and the peculiar social system of its bat host.     

Colony social structure in native and invasive populations of the social wasp Vespula pensylvanica

Social insects rank among the most invasive of terrestrial species. The success of invasive social insects stems, in part, from the flexibility derived from their social behaviors. We used genetic markers to investigate if the social system of the invasive wasp, Vespula pensylvanica, differed in its introduced and native habitats in order to better understand variation in social phenotype in invasive social species. We found that (1) nestmate workers showed lower levels of relatedness in introduced populations than native populations, (2) introduced colonies contained workers produced by multiple queens whereas native colonies contained workers produced by only a single queen, (3) queen mate number did not differ significantly between introduced and native colonies, and (4) workers from introduced colonies were frequently produced by queens that originated from foreign nests. Thus, overall, native and introduced colonies differed substantially in social phenotype because introduced colonies more frequently contained workers produced by multiple, foreign queens. In addition, the similarity in levels of genetic variation in introduced and native habitats, as well as observed variation in colony social phenotype in native populations, suggest that colony structure in invasive populations may be partially associated with social plasticity. Overall, the differences in social structure observed in invasive V. pensylvanica parallel those in other, distantly related invasive social insects, suggesting that insect societies often develop similar social phenotypes upon introduction into new habitats.     

Behavioral Plasticity in Ant Queens: Environmental Manipulation Induces Aggression among Normally Peaceful Queens in the Socially Polymorphic Ant Leptothorax acervorum

The behavioral traits that shape the structure of animal societies vary considerably among species but appear to be less flexible within species or at least within populations. Populations of the ant Leptothorax acervorum differ in how queens interact with other queens. Nestmate queens from extended, homogeneous habitats tolerate each other and contribute quite equally to the offspring of the colony (polygyny: low reproductive skew). In contrast, nestmate queens from patchy habitats establish social hierarchies by biting and antennal boxing, and eventually only the top-ranking queen of the colony lays eggs (functional monogyny: high reproductive skew). Here we investigate whether queen-queen behavior is fixed within populations or whether aggression and high skew can be elicited by manipulation of socio-environmental factors in colonies from low skew populations. An increase of queen/worker ratio and to a lesser extent food limitation elicited queen-queen antagonism in polygynous colonies from Nürnberger Reichswald similar to that underlying social and reproductive hierarchies in high-skew populations from Spain, Japan, and Alaska. In manipulated colonies, queens differed more in ovarian status than in control colonies. This indicates that queens are in principle capable of adapting the magnitude of reproductive skew to environmental changes in behavioral rather than evolutionary time.     

Spatial movement optimization in Amazonian <Emphasis Type="Italic">Eciton burchellii</Emphasis> army ants

Foraging army ants face a problem general to many animals—how best to confront resource depletion and environmental heterogeneity. Army ants have presumably evolved a nomadic lifestyle as a way to minimize re-exploitation of previously foraged areas. However, this solution creates a challenge for an army ant colony: foraging by this colony and others creates a shifting landscape of food resources, where colonies should theoretically avoid their own previous foraging paths as well as those of other colonies. Here, we examine how colonies exploit this resource mosaic, using some of the optimality arguments first proposed and tested by Franks and Fletcher (1983), but with much larger data sets in a new location in SW Amazonia. Our data supported Franks and Fletcher’s (1983) model for systematic avoidance of raided areas during the statary phase, as well as a hypothesis of distance optimization between successive statary bivouacs. We also test and find significant evidence that foraging raids turn in opposite directions from the previous day’s directional angles more frequently than what would be expected if turning angles were distributed at random, which acts to move a colony away from recently exploited areas. This implies that colonies follow a straighter line path during the nomadic phase as opposed to a curved one, which acts to maximize distance between statary bivouacs. In addition to intra-colony movement optimization, we examine evidence for inter-colony avoidance from more than 330 colony emigrations and suggest that colony-specific pheromones are not necessarily repulsive to other colonies. Lastly, we compare our results with those of similar studies carried out at Barro Colorado Island (BCI), Panama. Despite a higher density of army ants in the SW Amazon region, colonies spend less time emigrating than their counterparts at BCI, which suggests a higher prey density in SW Amazonia.     

Biannual birth pulses allow filoviruses to persist in bat populations

Filoviruses Ebolavirus (EBOV) and Marburgvirus (MARV) cause haemorrhagic fevers with high mortality rates, posing significant threats to public health. To understand transmission into human populations, filovirus dynamics within reservoir host populations must be understood. Studies have directly linked filoviruses to bats, but the mechanisms allowing viral persistence within bat populations are poorly understood. Theory suggests seasonal birthing may decrease the probability of pathogen persistence within populations, but data suggest MARV may persist within colonies of seasonally breeding Egyptian fruit bats, Rousettus aegyptiacus. I synthesize available filovirus and bat data in a stochastic compartmental model to explore fundamental questions relating to filovirus ecology: can filoviruses persist within isolated bat colonies; do critical community sizes exist; and how do host–pathogen relationships affect spillover transmission potential? Synchronous annual breeding and shorter incubation periods did not allow filovirus persistence, whereas bi-annual breeding and longer incubation periods, such as reported for Egyptian fruit bats and EBOV in experimental studies, allowed persistence in colony sizes often found in nature. Serological data support the findings, with bats from species with two annual birth pulses more likely to be seropositive (odds ratio (OR) 4.4, 95% confidence interval (CI) 2.5–8.7) than those with one, suggesting that biannual birthing is necessary for filovirus persistence.     

Altruistic self‐removal of health‐compromised honey bee workers from their hive

Social insect colonies represent distinct units of selection. Most individuals evolve by kin selection and forgo individual reproduction. Instead, they display altruistic food sharing, nest maintenance and self‐sacrificial colony defence. Recently, altruistic self‐removal of diseased worker ants from their colony was described as another important kin‐selected behaviour. Here, we report corroborating experimental evidence from honey bee foragers and theoretical analyses. We challenged honey bee foragers with prolonged CO₂ narcosis or by feeding with the cytostatic drug hydroxyurea. Both treatments resulted in increased mortality but also caused the surviving foragers to abandon their social function and remove themselves from their colony, resulting in altruistic suicide. A simple model suggests that altruistic self‐removal by sick social insect workers to prevent disease transmission is expected under most biologically plausible conditions. The combined theoretical and empirical support for altruistic self‐removal suggests that it may be another important kin‐selected behaviour and a potentially widespread mechanism of social immunity.     

The influence of social hunger on food distribution and its implications for disease transmission in a honeybee colony

Social insect colonies are characterized by extensive interactions among individuals, exchanges that can also potentially transmit pathogens. The large majority of these social interactions in a honeybee colony result from food transfer among individuals. Since colony hunger is likely to have a significant influence on these interactions, we investigated its effect on the distribution of food within the colony. By pulsing two colonies having different amounts of stored food with a radioactive label, we found that a starved colony sent out a larger number of foragers, brought in more food, and stored more of it than the satiated colony. We also found that the food brought into a starved colony was distributed more uniformly within each age class than that in the satiated colony. The queen and the young individuals received the lowest exposure to the label even though the label entered different regions of the colony at the same rate. The satiation level of the colony did not influence the relative exposures of different age groups to the label but a higher amount of it was stored in the hungry colony. We discuss the significance of these results in terms of the role played by the organizational structure of the honeybee colony on the transmission dynamics of an infectious disease.     

Early sexual dimorphism in the developing gut microbiome of northern elephant seals

The gut microbiome is an integral part of a species' ecology, but we know little about how host characteristics impact its development in wild populations. Here, we explored the role of such intrinsic factors in shaping the gut microbiome of northern elephant seals (Mirounga angustirostris) during a critical developmental window of 6 weeks after weaning, when the pups stay ashore without feeding. We found substantial sex differences in the early‐life gut microbiome, even though males and females could not yet be distinguished morphologically. Sex and age both explained around 15% of the variation in gut microbial beta diversity, while microbial communities sampled from the same individual showed high levels of similarity across time, explaining another 40% of the variation. Only a small proportion of the variation in beta diversity was explained by health status, assessed by full blood counts, but clinically healthy individuals had a greater microbial alpha diversity than their clinically abnormal peers. Across the post‐weaning period, the northern elephant seal gut microbiome was highly dynamic. We found evidence for several colonization and extinction events as well as a decline in Bacteroides and an increase in Prevotella, a pattern that has previously been associated with the transition from nursing to solid food. Lastly, we show that genetic relatedness was correlated with gut microbiome similarity in males but not females, again reflecting early sex differences. Our study represents a naturally diet‐controlled and longitudinal investigation of how intrinsic factors shape the early gut microbiome in a species with extreme sex differences in morphology and life history.     

An Insect Herbivore Microbiome with High Plant Biomass-Degrading Capacity

Herbivores can gain indirect access to recalcitrant carbon present in plant cell walls through symbiotic associations with lignocellulolytic microbes. A paradigmatic example is the leaf-cutter ant (Tribe: Attini), which uses fresh leaves to cultivate a fungus for food in specialized gardens. Using a combination of sugar composition analyses, metagenomics, and whole-genome sequencing, we reveal that the fungus garden microbiome of leaf-cutter ants is composed of a diverse community of bacteria with high plant biomass-degrading capacity. Comparison of this microbiome''s predicted carbohydrate-degrading enzyme profile with other metagenomes shows closest similarity to the bovine rumen, indicating evolutionary convergence of plant biomass degrading potential between two important herbivorous animals. Genomic and physiological characterization of two dominant bacteria in the fungus garden microbiome provides evidence of their capacity to degrade cellulose. Given the recent interest in cellulosic biofuels, understanding how large-scale and rapid plant biomass degradation occurs in a highly evolved insect herbivore is of particular relevance for bioenergy.     

Dispersal and group formation dynamics in a rare and endangered temperate forest bat (Nyctalus lasiopterus,Chiroptera: Vespertilionidae)

For elusive mammals like bats, colonization of new areas and colony formation are poorly understood, as is their relationship with the genetic structure of populations. Understanding dispersal and group formation behaviors is critical not only for a better comprehension of mammalian social dynamics, but also for guiding conservation efforts of rare and endangered species. Using nuclear and mitochondrial markers, we studied patterns of genetic diversity and differentiation among and within breeding colonies of giant noctule bats (Nyctalus lasiopterus), their relation to a new colony still in formation, and the impact of this ongoing process on the regionwide genetic makeup. Nuclear differentiation among colonies was relatively low and mostly nonsignificant. Mitochondrial variation followed this pattern, contrasting with findings for other temperate bat species. Our results suggest that this may indicate a recent population expansion. On average, female giant noctules were not more closely related to other colony members than to foreign individuals. This was also true for members of the newly forming colony and those of another, older group sampled shortly after its formation, suggesting that contrary to findings for other temperate bats, giant noctule colonies are not founded by relatives. However, mother–daughter pairs were found in the same populations more often than expected under random dispersal. Given this indication of philopatry, the lack of mitochondrial differentiation among most colonies in the region is probably due to the combination of a recent population expansion and group formation events.