Habituation of common vampire bats to biologgers.

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.

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.

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, whereas older techniques often still represent the state-of-the-art for studying small vertebrates. In industrial applications, low-power wireless sensor networks (WSNs) fulfill requirements similar to those needed to monitor animal behavior at high resolution and at low tag mass. We developed a wireless biologging network (WBN), which enables simultaneous direct proximity sensing, high-resolution tracking, and long-range remote data download at tag masses of 1 to 2 g. 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.

Development of New Food-Sharing Relationships in Vampire Bats.

Some nonhuman animals form adaptive long-term cooperative relationships with nonkin that seem analogous in form and function to human friendship [1-4]. However, it remains unclear how these bonds initially form, especially when they entail investments of time and energy. Theory suggests individuals can reduce the risk of exploitation by initially spreading out smaller cooperative investments across time [e.g., 5] or partners [6], then gradually escalating investments in more cooperative partnerships [7]. Despite its intuitive appeal, this raising-the-stakes model [7] has gained surprisingly scarce empirical support. Although human strangers do "raise the stakes" when making bids in cooperation games [8], there has been no clear evidence for raising the stakes during formation of social bonds in nature. Existing studies are limited to cooperative interactions with severe power asymmetries (e.g., the cleaner-client fish mutualism [9]) or snapshots of a single behavior within established relationships (grooming in primates [10-13]). Raising the stakes during relationship formation might involve escalating to more costly behaviors. For example, individuals could "test the waters" by first clustering for warmth (no cost), then conditionally grooming (low cost), and eventually providing coalitionary support (high cost). Detecting such a pattern requires introducing random strangers and measuring the emergence of natural helping behaviors that vary in costs. We performed this test by tracking the emergence of social grooming and regurgitated food donations among previously unfamiliar captive vampire bats (Desmodus rotundus) over 15 months. We found compelling evidence that vampire bats selectively escalate low-cost grooming before developing higher-cost food-sharing relationships.

Vampire Bats that Cooperate in the Lab Maintain Their Social Networks in the Wild.

Social bonds, maintained by mutual investments of time and energy, have greatly influenced the evolution of social cognition and cooperation in many species [e.g., 1-8]. However, there are two pitfalls regarding "social bonds" as an explanation for social structure and cooperation [1, 9-11]. First, studies often incorrectly assume that frequent association implies partner fidelity based on mutual social preference, but even seemingly complex nonrandom interaction networks can emerge solely from habitat or spatial structure [12-16]. Second, the false appearance of partner fidelity can result from stable options in the "partner market" [1, 9-11, 17]. For instance, individuals might preferentially groom the same partner, even if the decision depends entirely on the immediate costs and benefits rather than relationship history. Given these issues, a key challenge has been testing the extent to which social structure is driven by the intrinsic relationship history versus the extrinsic physical and social environment. If stable bonds exist, they should persist even if the individuals are moved to a dramatically different physical and social environment. We tested this prediction by tracking social relationships among common vampire bats (Desmodus rotundus) moved from the lab to the wild. We show that allogrooming and food sharing among female vampire bats induced in captivity over 22 months predicted their assortativity and association rates when we subsequently tracked them in the wild with custom-made high-resolution proximity sensors. The persistence of many relationships across different physical and social environments suggests that social structure is caused by both extrinsic constraints and intrinsic partner fidelity.

Nocturnal scent in a 'bird-fig': A cue to attract bats as additional dispersers?

The plant genus Ficus is a keystone resource in tropical ecoystems. One of the unique features of figs is the diversity of fruit traits, which in many cases match their various dispersers, the so-called fruit syndromes. The classic example of this is the strong phenotypic differences found between figs with bat and bird dispersers (color, size, presentation, and scent). The 'bird-fig' Ficus colubrinae represents an exception to this trend since it attracts the small frugivorous bat species Ectophylla alba at night, but during the day it attracts bird visitors. Here we investigate day to night changes in fruit scent as a possible mechanism by which this 'bird-fig' could attract bats despite its fruit traits, which should appeal solely to birds. Analyses of odor bouquets from the bat- and bird-dispersal phases (i.e. day and night) differed significantly in their composition of volatiles. We observed a significant increase in relative amounts of sesquiterpene and aromatic compounds at night while relative amounts of two compounds of the fatty acid pathway were significantly higher during day. This finding raises the question whether Ficus colubrinae, a phenotypically classic 'bird-fig', might be able to attract bat dispersers by an olfactory signal at night. Preliminary observations from feeding experiments which indicate that Ectophylla alba is capable of finding ripe figs by scent alone point in this direction. However, additional behavioral experiments on whether bats prefer the 'night-bouquet' over the 'day-bouquet' will be needed to unequivocally answer this question.

Movement seasonality in a desert-dwelling bat revealed by miniature GPS loggers.

BACKGROUND: Bats are among the most successful desert mammals. Yet, our understanding of their spatio-temporal dynamics in habitat use associated with the seasonal oscillation of resources is still limited. In this study, we have employed state-of-the-art lightweight GPS loggers to track the yellow-winged bat Lavia frons in a desert in northern Kenya to investigate how seasonality in a desert affects the a) spatial and b) temporal dimensions of movements in a low-mobility bat. METHODS: Bats were tracked during April-May 2017 (rainy season) and January-February 2018 (dry season) using 1-g GPS loggers. Spatial and temporal dimensions of movements were quantified, respectively, as the home range and nightly activity patterns. We tested for differences between seasons to assess responses to seasonal drought. In addition, we quantified home range overlap between neighbouring individuals to investigate whether tracking data will be in accordance with previous reports on territoriality and social monogamy in L. frons. RESULTS: We obtained data for 22 bats, 13 during the rainy and 9 during the dry season. Home ranges averaged 5.46 ± 11.04 ha and bats travelled a minimum distance of 99.69 ± 123.42 m/hour. During the dry season, home ranges were larger than in the rainy season, and bats exhibited high activity during most of the night. No apparent association with free water was identified during the dry season. The observed spatial organisation of home ranges supports previous observations that L. frons partitions the space into territories throughout the year. CONCLUSIONS: Our results suggest that, in low-mobility bats, a potential way to cope with seasonally harsh conditions and resource scarcity in deserts is to cover larger areas and increase time active, suggesting lower cost-efficiency of the foraging activity. Climate change may pose additional pressures on L. frons and other low-mobility species by further reducing food abundances.

Proximity sensors on common noctule bats reveal evidence that mothers guide juveniles to roosts but not food.

Female bats of temperate zones often communally rear their young, which creates ideal conditions for naive juveniles to find or learn about resources via informed adults. However, studying social information transfer in elusive and small-bodied animals in the wild is difficult with traditional tracking techniques. We used a novel 'next-generation' proximity sensor system (BATS) to investigate if and how juvenile bats use social information in acquiring access to two crucial resources: suitable roosts and food patches. By tracking juvenile-adult associations during roost switching and foraging, we found evidence for mother-to-offspring information transfer while switching roosts but not during foraging. Spatial and temporal patterns of encounters suggested that mothers guided juveniles between the juvenile and the target roost. This roost-switching behaviour provides evidence for maternal guidance in bats, a form of maternal care that has long been assumed, but never documented. We did not find evidence that mothers guide the offspring to foraging sites. Foraging bats reported brief infrequent meetings with other tagged bats that were best explained by local enhancement. Our study illustrates how this recent advance in automated biologging provides researchers with new insights into longstanding questions in behavioural biology.

Wireless Sensor Platform for Detection of Vital Parameters of Bats.

In this paper an advanced sensor node for animal tracking is proposed, which includes an accelerometer, an air pressure sensor as well as an electrocardiography sensor. The system is designed for studying the physiology and behavior of bats by inferring activity, wing beat frequency as well as heart rate. This system offers outstanding functionality compared to other tracking nodes and is easily applicable thanks to its noninvasive design. Gluing the sensor to the bat's back keeps the impact on the animal at a minimum and retrieval of the animal to remove the tag is not required since the tag falls off after a few days.

BATS: Adaptive Ultra Low Power Sensor Network for Animal Tracking.

In this paper, the BATS project is presented, which aims to track the behavior of bats via an ultra-low power wireless sensor network. An overview about the whole project and its parts like sensor node design, tracking grid and software infrastructure is given and the evaluation of the project is shown. The BATS project includes a lightweight sensor node that is attached to bats and combines multiple features. Communication among sensor nodes allows tracking of bat encounters. Flight trajectories of individual tagged bats can be recorded at high spatial and temporal resolution by a ground node grid. To increase the communication range, the BATS project implemented a long-range telemetry system to still receive sensor data outside the standard ground node network. The whole system is designed with the common goal of ultra-low energy consumption while still maintaining optimal measurement results. To this end, the system is designed in a flexible way and is able to adapt its functionality according to the current situation. In this way, it uses the energy available on the sensor node as efficient as possible.

Automated proximity sensing in small vertebrates: design of miniaturized sensor nodes and first field tests in bats.

Social evolution has led to a stunning diversity of complex social behavior, in particular in vertebrate taxa. Thorough documentation of social interactions is crucial to study the causes and consequences of sociality in gregarious animals. Wireless digital transceivers represent a promising tool to revolutionize data collection for the study of social interactions in terms of the degree of automation, data quantity, and quality. Unfortunately, devices for automated proximity sensing via direct communication among animal-borne sensors are usually heavy and do not allow for the investigation of small animal species, which represent the majority of avian and mammalian taxa. We present a lightweight animal-borne sensor node that is built from commercially available components and uses a sophisticated scheme for energy-efficient communication, with high sampling rates at relatively low power consumption. We demonstrate the basic functionality of the sensor node under laboratory conditions and its applicability for the study of social interactions among free-ranging animals. The first field tests were performed on two species of bats in temperate and tropical ecosystems. At <2 g, this sensor node is light enough to observe a broad spectrum of taxa including small vertebrates. Given our specifications, the system was especially sensitive to changes in distance within the short range (up to a distance of 4 m between tags). High spatial resolution at short distances enables the evaluation of interactions among individuals at a fine scale and the investigation of close contacts. This technology opens new avenues of research, allowing detailed investigation of events associated with social contact, such as mating behavior, pathogen transmission, social learning, and resource sharing. Social behavior that is not easily observed becomes observable, for example, in animals living in burrows or in nocturnal animals. A switch from traditional methods to the application of digital transceiver chips in proximity sensing offers numerous advantages in addition to an enormous increase in data quality and quantity. For future applications, the platform allows for the integration of additional sensors that may collect physiological or environmental data. Such information complements social network studies and may allow for a deeper understanding of animal ecology and social behavior.

Frugivorous bats maintain functional habitat connectivity in agricultural landscapes but rely strongly on natural forest fragments.

Anthropogenic changes in land use threaten biodiversity and ecosystem functioning by the conversion of natural habitat into agricultural mosaic landscapes, often with drastic consequences for the associated fauna. The first step in the development of efficient conservation plans is to understand movement of animals through complex habitat mosaics. Therefore, we studied ranging behavior and habitat use in Dermanura watsoni (Phyllostomidae), a frugivorous bat species that is a valuable seed disperser in degraded ecosystems. Radio-tracking of sixteen bats showed that the animals strongly rely on natural forest. Day roosts were exclusively located within mature forest fragments. Selection ratios showed that the bats foraged selectively within the available habitat and positively selected natural forest. However, larger daily ranges were associated with higher use of degraded habitats. Home range geometry and composition of focal foraging areas indicated that wider ranging bats performed directional foraging bouts from natural to degraded forest sites traversing the matrix over distances of up to three hundred meters. This behavior demonstrates the potential of frugivorous bats to functionally connect fragmented areas by providing ecosystem services between natural and degraded sites, and highlights the need for conservation of natural habitat patches within agricultural landscapes that meet the roosting requirements of bats.