A social foraging trade-off in echolocating bats reveals that they benefit from some conspecifics but are impaired when many are around.

Social foraging is very common in the animal kingdom. Numerous studies have documented collective foraging in various species and many reported the attraction of various species to foraging conspecifics. It is nonetheless difficult to quantify the benefits and costs of collective foraging, especially in the wild. We examined the benefits and costs of social foraging using on-board microphones mounted on freely foraging Molossus nigricans bats. This allowed us to quantify the bats' attacks on prey and to assess their success as a function of conspecific density. We found that the bats spent most of their time foraging at low conspecific densities, during which their attacks were most successful in terms of prey items captured per time unit. Notably, their capture rate dropped when conspecific density became either too high or too low. Our findings thus demonstrate a clear social foraging trade-off in which the presence of a few conspecifics probably improves foraging success, whereas the presence of too many impairs it.

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.

What determines the information update rate in echolocating bats.

The rate of sensory update is one of the most important parameters of any sensory system. The acquisition rate of most sensory systems is fixed and has been optimized by evolution to the needs of the animal. Echolocating bats have the ability to adjust their sensory update rate which is determined by the intervals between emissions - the inter-pulse intervals (IPI). The IPI is routinely adjusted, but the exact factors driving its regulation are unknown. We use on-board audio recordings to determine how four species of echolocating bats with different foraging strategies regulate their sensory update rate during commute flights. We reveal strong correlations between the IPI and various echolocation and movement parameters. Specifically, the update rate increases when the signals' peak-energy frequency and intensity increases while the update rate decreases when flight speed and altitude increases. We suggest that bats control their information update rate according to the behavioral mode they are engaged in, while always maintaining sensory continuity. Specifically, we suggest that bats apply two modes of attention during commute flights. Our data moreover suggests that bats emit echolocation signals at accurate intervals without the need for external feedback.

An artificial neural network explains how bats might use vision for navigation.

Animals navigate using various sensory information to guide their movement. Miniature tracking devices now allow documenting animals' routes with high accuracy. Despite this detailed description of animal movement, how animals translate sensory information to movement is poorly understood. Recent machine learning advances now allow addressing this question with unprecedented statistical learning tools. We harnessed this power to address visual-based navigation in fruit bats. We used machine learning and trained a convolutional neural network to navigate along a bat's route using visual information that would have been available to the real bat, which we collected using a drone. We show that a simple feed-forward network can learn to guide the agent towards a goal based on sensory input, and can generalize its learning both in time and in space. Our analysis suggests how animals could potentially use visual input for navigation and which features might be useful for this purpose.

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.

Fruit bats adjust their foraging strategies to urban environments to diversify their diet.

BACKGROUND: Urbanization is one of the most influential processes on our globe, putting a great number of species under threat. Some species learn to cope with urbanization, and a few even benefit from it, but we are only starting to understand how they do so. In this study, we GPS tracked Egyptian fruit bats from urban and rural populations to compare their movement and foraging in urban and rural environments. Because fruit trees are distributed differently in these two environments, with a higher diversity in urban environments, we hypothesized that foraging strategies will differ too. RESULTS: When foraging in urban environments, bats were much more exploratory than when foraging in rural environments, visiting more sites per hour and switching foraging sites more often on consecutive nights. By doing so, bats foraging in settlements diversified their diet in comparison to rural bats, as was also evident from their choice to often switch fruit species. Interestingly, the location of the roost did not dictate the foraging grounds, and we found that many bats choose to roost in the countryside but nightly commute to and forage in urban environments. CONCLUSIONS: Bats are unique among small mammals in their ability to move far rapidly. Our study is an excellent example of how animals adjust to environmental changes, and it shows how such mobile mammals might exploit the new urban fragmented environment that is taking over our landscape.

Fireflies produce ultrasonic clicks during flight as a potential aposematic anti-bat signal.

Fireflies are known for emitting light signals for intraspecific communication. However, in doing so, they reveal themselves to many potential nocturnal predators from a large distance. Therefore, many fireflies evolved unpalatable compounds and probably use their light signals as anti-predator aposematic signals. Fireflies are occasionally attacked by predators despite their warning flashes. Bats are among the most substantial potential firefly predators. Using their echolocation, bats might detect a firefly from a short distance and attack it in between two flashes. We thus aimed to examine whether fireflies use additional measures of warning, specifically focusing on sound signals. We recorded four species from different genera of fireflies in Vietnam and Israel and found that all of them generated ultrasonic clicks centered around bats' hearing range. Clicks were synchronized with the wingbeat and are probably produced by the wings. We hypothesize that ultrasonic clicks can serve as part of a multimodal aposematic display.

Echolocating bats can adjust sensory acquisition based on internal cues.

BACKGROUND: Sensory systems acquire both external and internal information to guide behavior. Adjustments based on external input are much better documented and understood than internal-based sensory adaptations. When external input is not available, idiothetic-internal-cues become crucial for guiding behavior. Here, we take advantage of the rapid sensory adjustments exhibited by bats in order to study how animals rely on internal cues in the absence of external input. Constant frequency echolocating bats are renowned for their Doppler shift compensation response used to adjust their emission frequency in order to optimize sensing. Previous studies documented the importance of external echoes for this response. RESULTS: We show that the Doppler compensation system works even without external feedback. Bats experiencing accelerations in an echo-free environment exhibited an intact compensation response. Moreover, using on-board GPS tags on free-flying bats in the wild, we demonstrate that the ability to perform Doppler shift compensation response based on internal cues might be essential in real-life when echo feedback is not available. CONCLUSIONS: We thus show an ecological need for using internal cues as well as an ability to do so. Our results illustrate the robustness of one particular sensory behavior; however, we suggest this ability to rely on different streams of information (i.e., internal or external) is probably relevant for many sensory behaviors.

Echolocating bats detect but misperceive a multidimensional incongruent acoustic stimulus.

Coherent perception relies on integrating multiple dimensions of a sensory modality, for example, color and shape in vision. We reveal how different acoustic dimensions, specifically echo intensity and sonar aperture (or width), are important for correct perception by echolocating bats. We flew bats down a corridor blocked by objects with different intensity-aperture combinations. To our surprise, bats crashed straight into large (aperture) walls with weak echo intensity as if they did not exist. The echolocation behavior of the bats indicated that they did detect the wall, suggesting that crashing was not a result of limited sensory sensitivity, but of a perceptual deficit. We systematically manipulated intensity and aperture by changing the materials and width of different reflectors, and we conclude that a coherent echo-based percept is created only when these two acoustic dimensions have certain relations which are typical for objects in nature (e.g., large and intense or small and weak reflectors). Nevertheless, we show that these preferred relations are not innate. We show that young pups are not constrained to these relations and that new intensity-aperture associations can also be learned by adult bats.

Reinforcement Learning Enables Resource Partitioning in Foraging Bats.

Every evening, from late spring to mid-summer, tens of thousands of hungry lactating female lesser long-nosed bats (Leptonycteris yerbabuenae) emerge from their roost and navigate over the Sonoran Desert, seeking for nectar and pollen [1, 2]. The bats roost in a huge maternal colony that is far from the foraging grounds but allows their pups to thermoregulate [3] while the mothers are foraging. Thus, the mothers have to fly tens of kilometers to the foraging sites-fields with thousands of Saguaro cacti [4, 5]. Once at the field, they must compete with many other bats over the same flowering cacti. Several solutions have been suggested for this classical foraging task of exploiting a resource composed of many renewable food sources whose locations are fixed. Some animals randomly visit the food sources [6], and some actively defend a restricted foraging territory [7-11] or use simple forms of learning, such as "win-stay lose-switch" strategy [12]. Many species have been suggested to follow a trapline, that is, to revisit the food sources in a repeating ordered manner [13-22]. We thus hypothesized that lesser long-nosed bats would visit cacti in a sequenced manner. Using miniature GPS devices, aerial imaging, and video recordings, we tracked the full movement of the bats and all of their visits to their natural food sources. Based on real data and evolutionary simulations, we argue that the bats use a reinforcement learning strategy that requires minimal memory to create small, non-overlapping cacti-cores and exploit nectar efficiently, without social communication.

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.

Plants' ability to sense and respond to airborne sound is likely to be adaptive: reply to comment by Pyke et al.

Ecol. Lett. 22, 2019, 1483 demonstrated, for the first time, a rapid response of a plant to the airborne sounds of pollinators. Pyke et al. argue that this response is unlikely to be adaptive. Here we clarify some misunderstandings, and demonstrate the potential adaptive value using theoretical modelling and field observations.

Flowers respond to pollinator sound within minutes by increasing nectar sugar concentration.

Can plants sense natural airborne sounds and respond to them rapidly? We show that Oenothera drummondii flowers, exposed to playback sound of a flying bee or to synthetic sound signals at similar frequencies, produce sweeter nectar within 3 min, potentially increasing the chances of cross pollination. We found that the flowers vibrated mechanically in response to these sounds, suggesting a plausible mechanism where the flower serves as an auditory sensory organ. Both the vibration and the nectar response were frequency-specific: the flowers responded and vibrated to pollinator sounds, but not to higher frequency sound. Our results document for the first time that plants can rapidly respond to pollinator sounds in an ecologically relevant way. Potential implications include plant resource allocation, the evolution of flower shape and the evolution of pollinators sound. Finally, our results suggest that plants may be affected by other sounds as well, including anthropogenic ones.

Interspecific variation in the relationship between clutch size, laying date and intensity of urbanization in four species of hole-nesting birds.

The increase in size of human populations in urban and agricultural areas has resulted in considerable habitat conversion globally. Such anthropogenic areas have specific environmental characteristics, which influence the physiology, life history, and population dynamics of plants and animals. For example, the date of bud burst is advanced in urban compared to nearby natural areas. In some birds, breeding success is determined by synchrony between timing of breeding and peak food abundance. Pertinently, caterpillars are an important food source for the nestlings of many bird species, and their abundance is influenced by environmental factors such as temperature and date of bud burst. Higher temperatures and advanced date of bud burst in urban areas could advance peak caterpillar abundance and thus affect breeding phenology of birds. In order to test whether laying date advance and clutch sizes decrease with the intensity of urbanization, we analyzed the timing of breeding and clutch size in relation to intensity of urbanization as a measure of human impact in 199 nest box plots across Europe, North Africa, and the Middle East (i.e., the Western Palearctic) for four species of hole-nesters: blue tits (Cyanistes caeruleus), great tits (Parus major), collared flycatchers (Ficedula albicollis), and pied flycatchers (Ficedula hypoleuca). Meanwhile, we estimated the intensity of urbanization as the density of buildings surrounding study plots measured on orthophotographs. For the four study species, the intensity of urbanization was not correlated with laying date. Clutch size in blue and great tits does not seem affected by the intensity of urbanization, while in collared and pied flycatchers it decreased with increasing intensity of urbanization. This is the first large-scale study showing a species-specific major correlation between intensity of urbanization and the ecology of breeding. The underlying mechanisms for the relationships between life history and urbanization remain to be determined. We propose that effects of food abundance or quality, temperature, noise, pollution, or disturbance by humans may on their own or in combination affect laying date and/or clutch size.

Variation in clutch size in relation to nest size in birds.

Nests are structures built to support and protect eggs and/or offspring from predators, parasites, and adverse weather conditions. Nests are mainly constructed prior to egg laying, meaning that parent birds must make decisions about nest site choice and nest building behavior before the start of egg-laying. Parent birds should be selected to choose nest sites and to build optimally sized nests, yet our current understanding of clutch size-nest size relationships is limited to small-scale studies performed over short time periods. Here, we quantified the relationship between clutch size and nest size, using an exhaustive database of 116 slope estimates based on 17,472 nests of 21 species of hole and non-hole-nesting birds. There was a significant, positive relationship between clutch size and the base area of the nest box or the nest, and this relationship did not differ significantly between open nesting and hole-nesting species. The slope of the relationship showed significant intraspecific and interspecific heterogeneity among four species of secondary hole-nesting species, but also among all 116 slope estimates. The estimated relationship between clutch size and nest box base area in study sites with more than a single size of nest box was not significantly different from the relationship using studies with only a single size of nest box. The slope of the relationship between clutch size and nest base area in different species of birds was significantly negatively related to minimum base area, and less so to maximum base area in a given study. These findings are consistent with the hypothesis that bird species have a general reaction norm reflecting the relationship between nest size and clutch size. Further, they suggest that scientists may influence the clutch size decisions of hole-nesting birds through the provisioning of nest boxes of varying sizes.