Time-mapping and future-oriented behavior in free-ranging wild fruit bats.

Episodic memory and mental time travel have been viewed as uniquely human traits.1,2,3 This view began to shift with the development of behavioral criteria to assess what is referred to as "episodic-like memory" in animals.4,5 Key findings have ranged from evidence of what-where-when memory in scrub-jays, rats, and bees; through decision-making that impacts future foraging in frugivorous primates; to evidence of planning based on future needs in scrub-jays and tool use planning in great apes.4,6,7,8,9,10,11,12,13 Field studies of these issues have been rare, though there is field-based evidence for future-oriented behaviors in primates.8,10,14,15 We report evidence that free-ranging wild fruit bats rely on mental temporal maps and exhibit future-oriented behaviors when foraging. We tracked young bats as they navigated and foraged, documenting every tree they visited over many months. We prevented the bats from foraging outside for different time periods and monitored their foraging decisions, revealing that the bats map the spatiotemporal patterns of resources in their environment. Following a long period in captivity, the bats did not visit those trees that were no longer providing fruit. We show that this time-mapping ability requires experience and is lacking in inexperienced bats. Careful analysis of the bats' movement and foraging choices indicated that they plan which tree to visit while still in the colony, thus exhibiting future-oriented behavior and delayed gratification on a nightly basis. Our findings demonstrate how the need for spatiotemporal mental mapping can drive the evolution of high cognitive abilities that were previously considered exclusive to humans.

Mother bats facilitate pup navigation learning.

Learning where to forage and how to navigate to foraging sites are among the most essential skills that infants must acquire. How they do so is poorly understood. Numerous bat species carry their young in flight while foraging. This behavior is costly, and the benefits for the offspring are not fully clear. Using GPS tracking of both mothers and bat pups, we documented the pups' ontogeny from being non-volant to foraging independently. Our results suggest that mothers facilitate learning of navigation, assisting their pups with future foraging, by repeatedly placing them on specific trees and by behaving in a manner that seemed to encourage learning. Once independent, pups first flew alone to the same sites that they were carried to by their mothers, following similar routes used by their mothers, after which they began exploring new sites. Notably, in our observations, pups never independently followed their mothers in flight but were always carried by them, suggesting that learning occurred while passively being transported upside down.

Urban bat pups take after their mothers and are bolder and faster learners than rural pups.

BACKGROUND: Urbanization is rapidly changing our planet and animals that live in urban environments must quickly adjust their behavior. One of the most prevalent behavioral characteristics of urban dwelling animals is an increased level of risk-taking. Here, we aimed to reveal how urban fruitbats become risk-takers, and how they differ behaviorally from rural bats, studying both genetic and non-genetic factors that might play a role in the process. We assessed the personality of newborn pups from both rural and urban colonies before they acquired experience outdoors, examining risk-taking, exploration, and learning rates. RESULTS: Urban pups exhibited significantly higher risk-taking levels, they were faster learners, but less exploratory than their rural counterparts. A cross-fostering experiment revealed that pups were more similar to their adoptive mothers, thus suggesting a non-genetic mechanism and pointing towards a maternal effect. We moreover found that lactating urban mothers have higher cortisol levels in their milk, which could potentially explain the transmission of some personality traits from mother to pup. CONCLUSIONS: Young bats seem to acquire environment suitable traits via post-birth non-genetic maternal effects. We offer a potential mechanism for how urban pups can acquire urban-suitable behavioral traits through hormonal transfer from their mothers.

Sick bats stay home alone: fruit bats practice social distancing when faced with an immunological challenge.

Along with its many advantages, social roosting imposes a major risk of pathogen transmission. How social animals reduce this risk is poorly documented. We used lipopolysaccharide challenge to imitate bacterial infection in both a captive and a free-living colony of an extremely social, long-lived mammal-the Egyptian fruit bat. We monitored behavioral and physiological responses using an arsenal of methods, including onboard GPS to track foraging, acceleration sensors to monitor movement, infrared video to record social behavior, and blood samples to measure immune markers. Sick-like (immune-challenged) bats exhibited an increased immune response, as well as classic illness symptoms, including fever, weight loss, anorexia, and lethargy. Notably, the bats also exhibited behaviors that would reduce pathogen transfer. They perched alone and appeared to voluntarily isolate themselves from the group by leaving the social cluster, which is extremely atypical for this species. The sick-like individuals in the open colony ceased foraging outdoors for at least two nights, thus reducing transmission to neighboring colonies. Together, these sickness behaviors demonstrate a strong, integrative immune response that promotes recovery of infected individuals while reducing pathogen transmission inside and outside the roost, including spillover events to other species, such as humans.

The ontogeny of a mammalian cognitive map in the real world.

How animals navigate over large-scale environments remains a riddle. Specifically, it is debated whether animals have cognitive maps. The hallmark of map-based navigation is the ability to perform shortcuts, i.e., to move in direct but novel routes. When tracking an animal in the wild, it is extremely difficult to determine whether a movement is truly novel because the animal's past movement is unknown. We overcame this difficulty by continuously tracking wild fruit bat pups from their very first flight outdoors and over the first months of their lives. Bats performed truly original shortcuts, supporting the hypothesis that they can perform large-scale map-based navigation. We documented how young pups developed their visual-based map, exemplifying the importance of exploration and demonstrating interindividual differences.

Food for Sex in Bats Revealed as Producer Males Reproduce with Scrounging Females.

Food sharing is often evolutionarily puzzling, because the provider's benefits are not always clear. Sharing among kin may increase indirect fitness [1], but when non-kin are involved, different mechanisms were suggested to act. Occasionally, "tolerated theft" [2, 3] is observed, merely because defending a resource is not cost effective. Sharing may also be explained as "costly signaling" [4, 5], where individuals signal their high qualities by distributing acquired resources, as has been suggested to occur in certain human cultures [6]. Alternatively, a transferred food item might be compensated for in later interactions [7]. In vampire bats, blood sharing reflects reciprocity between non-kin colony members [8-10], and long-term social bonds affect food sharing in chimpanzees [11]. Food may also be exchanged for other goods or social benefits [12-14]. One reciprocity-based explanation for intersexual food sharing is the food-for-sex hypothesis [15-17]. This hypothesis proposes that males share food with females in exchange for mating opportunities. Studies on human hunter-gatherer societies suggest that males with increased foraging success have higher reproductive success [18, 19]. Male chimpanzees, which in contrast to humans do not maintain pair bonds, were suggested to share food with females to increase their mating opportunities [16] (but see [20]). Bats, which are long-lived social mammals [21, 22], provide an opportunity to study long-term social reciprocity mechanisms. We monitored producer-scrounger interactions of a captive Egyptian fruit bat (Rousettus aegyptiacus) colony for more than a year and genetically determined the paternity of the pups that were born in the colony. We found that females carry the young of males from which they used to scrounge food, supporting the food-for-sex hypothesis in this species.

Coordinated change at the colony level in fruit bat fur microbiomes through time.

The host-associated microbiome affects individual health and behaviour, and may be influenced by local environmental conditions. However, little is known about microbiomes' temporal dynamics in free-living species compared with their dynamics in humans and model organisms, especially in body sites other than the gut. Here, we investigate longitudinal changes in the fur microbiome of captive and free-living Egyptian fruit bats. We find that, in contrast to patterns described in humans and other mammals, the prominent dynamics is of change over time at the level of the colony as a whole. On average, a pair of fur microbiome samples from different individuals in the same colony collected on the same date are more similar to one another than a pair of samples from the same individual collected at different time points. This pattern suggests that the whole colony may be the appropriate biological unit for understanding some of the roles of the host microbiome in social bats' ecology and evolution. This pattern of synchronized colony changes over time is also reflected in the profile of volatile compounds in the bats' fur, but differs from the more individualized pattern found in the bats' gut microbiome.

Resource Ephemerality Drives Social Foraging in Bats.

Observations of animals feeding in aggregations are often interpreted as events of social foraging, but it can be difficult to determine whether the animals arrived at the foraging sites after collective search [1-4] or whether they found the sites by following a leader [5, 6] or even independently, aggregating as an artifact of food availability [7, 8]. Distinguishing between these explanations is important, because functionally, they might have very different consequences. In the first case, the animals could benefit from the presence of conspecifics, whereas in the second and third, they often suffer from increased competition [3, 9-13]. Using novel miniature sensors, we recorded GPS tracks and audio of five species of bats, monitoring their movement and interactions with conspecifics, which could be inferred from the audio recordings. We examined the hypothesis that food distribution plays a key role in determining social foraging patterns [14-16]. Specifically, this hypothesis predicts that searching for an ephemeral resource (whose distribution in time or space is hard to predict) is more likely to favor social foraging [10, 13-15] than searching for a predictable resource. The movement and social interactions differed between bats foraging on ephemeral versus predictable resources. Ephemeral species changed foraging sites and showed large temporal variation nightly. They aggregated with conspecifics as was supported by playback experiments and computer simulations. In contrast, predictable species were never observed near conspecifics and showed high spatial fidelity to the same foraging sites over multiple nights. Our results suggest that resource (un)predictability influences the costs and benefits of social foraging.

Persistent producer-scrounger relationships in bats.

Social foraging theory suggests that group-living animals gain from persistent social bonds, which lead to increased tolerance in competitive foraging and information sharing. Bats are among the most social mammals, often living in colonies of tens to thousands of individuals for dozens of years, yet little is known about their social foraging dynamics. We observed three captive bat colonies for over a year, quantifying >13,000 social foraging interactions. We found that individuals consistently used one of two foraging strategies, either producing (collecting) food themselves or scrounging it directly from the mouth of other individuals. Individual foraging types were consistent over at least 16 months except during the lactation period when females shifted toward producing. Scroungers intentionally selected whom to interact with when socially foraging, thus generating persistent nonrandom social relationships with two to three specific producers. These persistent producer-scrounger relationships seem to reduce aggression over time. Finally, scrounging was highly correlated with vigilance, and we hypothesize that vigilant-prone individuals turn to scrounging in the wild to mitigate the risk of landing on a potentially unsafe fruit tree. We find the bat colony to be a rich and dynamic social system, which can serve as a model to study the role that social foraging plays in the evolution of mammalian sociality. Our results highlight the importance of considering individual tendencies when exploring social behavior patterns of group-living animals. These tendencies further emphasize the necessity of studying social networks over time.