A robotic falcon induces similar collective escape responses in different bird species.

Patterns of collective escape of a bird flock from a predator are fascinating, but difficult to study under natural conditions because neither prey nor predator is under experimental control. We resolved this problem by using an artificial predator (RobotFalcon) resembling a peregrine falcon in morphology and behaviour. We imitated hunts by chasing flocks of corvids, gulls, starlings and lapwings with the RobotFalcon, and compared their patterns of collective escape to those when chased by a conventional drone and, in case of starlings, hunted by wild peregrine falcons. Active pursuit of flocks, rather than only flying nearby by either the RobotFalcon or the drone, made flocks collectively escape more often. The RobotFalcon elicited patterns of collective escape in flocks of all species more often than the drone. Attack altitude did not affect the frequency of collective escape. Starlings escaped collectively equally often when chased by the RobotFalcon or a wild peregrine falcon. Flocks of all species reacted most often by collective turns, second most often by compacting and third by splitting into subflocks. This study demonstrates the potential of an artificial aerial predator for studying the collective escape behaviour of free-living birds, opening exciting avenues in the empirical study of prey-predator interactions.

Deterrence of birds with an artificial predator, the RobotFalcon.

Collisions between birds and airplanes can damage aircrafts, resulting in delays and cancellation of flights, costing the international civil aviation industry more than 1.4 billion US dollars annually. Driving away birds is therefore crucial, but the effectiveness of current deterrence methods is limited. Live avian predators can be an effective deterrent, because potential prey will not habituate to them, but live predators cannot be controlled entirely. Thus, there is an urgent need for new deterrence methods. We developed the RobotFalcon, a device modelled after the peregrine falcon, and tested its effectiveness to deter flocks of corvids, gulls, starlings and lapwings. We compared its effectiveness with that of a drone, and of conventional methods routinely applied at a military airbase. The RobotFalcon scared away bird flocks from fields immediately, and these fields subsequently remained free of bird flocks for hours. The RobotFalcon outperformed the drone and the best conventional method at the airbase (distress calls). Importantly, there was no evidence that bird flocks habituated to the RobotFalcon over the course of the fieldwork. We conclude that the RobotFalcon is a practical and ethical solution to drive away bird flocks with all advantages of live predators but without their limitations.

Gossip promotes cooperation only when it is pro-socially motivated.

Humans are often shown to cooperate with one another. Most of the mechanisms that foster cooperation among humans rely on reputation, which itself relies on the acquisition of information about other people's behaviors. Gossip has been proposed as a cheap yet efficient tool to acquire information, and it has largely been proved to be an effective means to foster and maintain cooperation. However, empirical studies supporting this claim have ignored two aspects: (1) they often compared gossip to treatments in which no reputation was available, impeding a direct assessment of whether it is gossip that promotes cooperation or rather the introduction of a reputation system; and (2) they focused on pro-social gossip (e.g., gossip aimed at helping the receiver), neglecting the impact of other types of gossip. We show here that, in contrast with the widespread notion that gossip promotes cooperation, gossip mostly depletes cooperation compared to first-hand information. If lying is fruitful for individuals or if a group's behavior is largely uncooperative, gossip leads to negative reputational information and decreased cooperation.

Emergence of splits and collective turns in pigeon flocks under predation.

Complex patterns of collective behaviour may emerge through self-organization, from local interactions among individuals in a group. To understand what behavioural rules underlie these patterns, computational models are often necessary. These rules have not yet been systematically studied for bird flocks under predation. Here, we study airborne flocks of homing pigeons attacked by a robotic falcon, combining empirical data with a species-specific computational model of collective escape. By analysing GPS trajectories of flocking individuals, we identify two new patterns of collective escape: early splits and collective turns, occurring even at large distances from the predator. To examine their formation, we extend an agent-based model of pigeons with a 'discrete' escape manoeuvre by a single initiator, namely a sudden turn interrupting the continuous coordinated motion of the group. Both splits and collective turns emerge from this rule. Their relative frequency depends on the angular velocity and position of the initiator in the flock: sharp turns by individuals at the periphery lead to more splits than collective turns. We confirm this association in the empirical data. Our study highlights the importance of discrete and uncoordinated manoeuvres in the collective escape of bird flocks and advocates the systematic study of their patterns across species.

Self-organization of collective escape in pigeon flocks.

Bird flocks under predation demonstrate complex patterns of collective escape. These patterns may emerge by self-organization from local interactions among group-members. Computational models have been shown to be valuable for identifying what behavioral rules may govern such interactions among individuals during collective motion. However, our knowledge of such rules for collective escape is limited by the lack of quantitative data on bird flocks under predation in the field. In the present study, we analyze the first GPS trajectories of pigeons in airborne flocks attacked by a robotic falcon in order to build a species-specific model of collective escape. We use our model to examine a recently identified distance-dependent pattern of collective behavior: the closer the prey is to the predator, the higher the frequency with which flock members turn away from it. We first extract from the empirical data of pigeon flocks the characteristics of their shape and internal structure (bearing angle and distance to nearest neighbors). Combining these with information on their coordination from the literature, we build an agent-based model adjusted to pigeons' collective escape. We show that the pattern of turning away from the predator with increased frequency when the predator is closer arises without prey prioritizing escape when the predator is near. Instead, it emerges through self-organization from a behavioral rule to avoid the predator independently of their distance to it. During this self-organization process, we show how flock members increase their consensus over which direction to escape and turn collectively as the predator gets closer. Our results suggest that coordination among flock members, combined with simple escape rules, reduces the cognitive costs of tracking the predator while flocking. Such escape rules that are independent of the distance to the predator can now be investigated in other species. Our study showcases the important role of computational models in the interpretation of empirical findings of collective behavior.

Absence of "selfish herd" dynamics in bird flocks under threat.

The "selfish herd" hypothesis1 provides a potential mechanism to explain a ubiquitous phenomenon in nature: that of non-kin aggregations. Individuals in selfish herds are thought to benefit by reducing their own risk at the expense of conspecifics by attracting toward their neighbors' positions1,2 or central locations in the aggregation.3-5 Alternatively, increased alignment with their neighbors' orientation could reduce the chance of predation through information sharing6-8 or collective escape.6 Using both small and large flocks of homing pigeons (Columba livia; n = 8-10 or n = 27-34 individuals) tagged with 5-Hz GPS loggers and a GPS-tagged, remote-controlled model peregrine falcon (Falco peregrinus), we tested whether individuals increase their use of attraction over alignment when under perceived threat. We conducted n = 27 flights in treatment conditions, chased by the robotic "predator," and n = 16 flights in control conditions (not chased). Despite responding strongly to the RobotFalcon-by turning away from its flight direction-individuals in treatment flocks demonstrated no increased attraction compared with control flocks, and this result held across both flock sizes. We suggest that mutualistic alignment is more advantageous than selfish attraction in groups with a high coincidence of individual and collective interests (adaptive hypothesis). However, we also explore alternative explanations, such as high cognitive demand under threat and collision avoidance (mechanistic hypotheses). We conclude that selfish herd may not be an appropriate paradigm for understanding the function of highly synchronous collective motion, as observed in bird flocks and perhaps also fish shoals and highly aligned mammal aggregations, such as moving herds.

Female emancipation in a male dominant, sexually dimorphic primate under natural conditions.

In most group-living animals, a dominance hierarchy reduces the costs of competition for limited resources. Dominance ranks may reflect prior attributes, such as body size, related to fighting ability or reflect the history of self-reinforcing effects of winning and losing a conflict (the winner-loser effect), or both. As to prior attributes, in sexually dimorphic species, where males are larger than females, males are assumed to be dominant over females. As to the winner-loser effect, the computational model DomWorld has shown that despite the female's lower initial fighting ability, females achieve some degree of dominance of females over males. In the model, this degree of female dominance increases with the proportion of males in a group. This increase was supposed to emerge from the higher fraction of fights of males among themselves. These correlations were confirmed in despotic macaques, vervet monkeys, and in humans. Here, we first investigate this hypothesis in DomWorld and next in long-term data of 9,300 observation hours on six wild groups of robust capuchin monkeys (Sapajus libidinosus; S. nigritus, and S. xanthosternos) in three Brazilian sites. We test whether both the proportion of males and degree of female dominance over males are indeed associated with a higher relative frequency of aggression among males and a higher relative frequency of aggression of females to males. We confirm these correlations in DomWorld. Next, we confirm in empirical data of capuchin monkeys that with the proportion of males in the group there is indeed an increase in female dominance over males, and in the relative frequency of both male-male aggression and aggression of females to males and that the female dominance index is significantly positively associated with male male aggression. Our results reveal that adult sex ratio influences the power relation between the sexes beyond predictions from socioecological models.

The 2020 motile active matter roadmap.

Activity and autonomous motion are fundamental in living and engineering systems. This has stimulated the new field of 'active matter' in recent years, which focuses on the physical aspects of propulsion mechanisms, and on motility-induced emergent collective behavior of a larger number of identical agents. The scale of agents ranges from nanomotors and microswimmers, to cells, fish, birds, and people. Inspired by biological microswimmers, various designs of autonomous synthetic nano- and micromachines have been proposed. Such machines provide the basis for multifunctional, highly responsive, intelligent (artificial) active materials, which exhibit emergent behavior and the ability to perform tasks in response to external stimuli. A major challenge for understanding and designing active matter is their inherent nonequilibrium nature due to persistent energy consumption, which invalidates equilibrium concepts such as free energy, detailed balance, and time-reversal symmetry. Unraveling, predicting, and controlling the behavior of active matter is a truly interdisciplinary endeavor at the interface of biology, chemistry, ecology, engineering, mathematics, and physics. The vast complexity of phenomena and mechanisms involved in the self-organization and dynamics of motile active matter comprises a major challenge. Hence, to advance, and eventually reach a comprehensive understanding, this important research area requires a concerted, synergetic approach of the various disciplines. The 2020 motile active matter roadmap of Journal of Physics: Condensed Matter addresses the current state of the art of the field and provides guidance for both students as well as established scientists in their efforts to advance this fascinating area.

Sexual size dimorphism, prey morphology and catch success in relation to flight mechanics in the peregrine falcon: a simulation study.

In common with many other raptors, female peregrine falcons Falco peregrinus are about 50% heavier than males. Their sexual dimorphism is thought to allow breeding pairs to exploit a wider range of prey through a division of labor: the male being able to catch more maneuverable prey species; the female capable of carrying larger ones. Given the difficulty of assessing the catch success and load carrying capacity of both sexes of falcon in the field, we here adopt a novel approach to test the division-of-labor theory by using a detailed physics-based flight simulator of birds. We study attacks by male and female peregrines on prey species ranging from small passerines to large ducks, testing how catch success relates to the flight performance of predator and prey. Males prove to be better than females at catching highly maneuverable prey in level flight, but the catch success of both sexes improves and becomes more similar when diving, because of the higher aerodynamic forces that are available to both sexes for maneuvering in high-speed flight. The higher maximum roll acceleration of the male peregrine explains its edge over the female in catching maneuverable prey in level flight. Overall, catch success is more strongly influenced by the differences in maneuverability that exist between different species of prey than between the different sexes of falcon. On the other hand, the female can carry up to 50% greater loads than the male. More generally, our detailed simulation approach highlights the importance of several previously overlooked features of attack and escape. In particular, we find that it is not the prey's instantaneous maximum centripetal acceleration but the prey's ability to sustain a high centripetal acceleration for an extended period of time that is the primary driver of the variation in catch success across species.

Young macaques (Macaca fascicularis) preferentially bias attention towards closer, older, and better tool users.

Examining how animals direct social learning during skill acquisition under natural conditions, generates data for examining hypotheses regarding how transmission biases influence cultural change in animal populations. We studied a population of macaques on Koram Island, Thailand, and examined model-based biases during interactions by unskilled individuals with tool-using group members. We first compared the prevalence of interactions (watching, obtaining food, object exploration) and proximity to tool users during interactions, in developing individuals (infants, juveniles) versus mature non-learners (adolescents, adults), to provide evidence that developing individuals are actively seeking information about tool use from social partners. All infants and juveniles, but only 49% of mature individuals carried out interacted with tool users. Macaques predominantly obtained food by scrounging or stealing, suggesting maximizing scrounging opportunities motivates interactions with tool users. However, while interactions by adults was limited to obtaining food, young macaques and particularly infants also watched tool users and explored objects, indicating additional interest in tool use itself. We then ran matrix correlations to identify interaction biases, and what attributes of tool users influenced these. Biases correlated with social affiliation, but macaques also preferentially targeted tool users that potentially increase scrounging and learning opportunities. Results suggest that social structure may constrain social learning, but the motivation to bias interactions towards tool users to maximize feeding opportunities may also socially modulate learning by facilitating close proximity to better tool users, and further interest in tool-use actions and materials, especially during development.

Social conformity and propagation of information in collective U-turns of fish schools.

Moving animal groups such as schools of fishes or flocks of birds often undergo sudden collective changes of their travelling direction as a consequence of stochastic fluctuations in heading of the individuals. However, the mechanisms by which these behavioural fluctuations arise at the individual level and propagate within a group are still unclear. In this study, we combine an experimental and theoretical approach to investigate spontaneous collective U-turns in groups of rummy-nose tetra (Hemigrammus rhodostomus) swimming in a ring-shaped tank. U-turns imply that fish switch their heading between the clockwise and anticlockwise direction. We reconstruct trajectories of individuals moving alone and in groups of different sizes. We show that the group decreases its swimming speed before a collective U-turn. This is in agreement with previous theoretical predictions showing that speed decrease facilitates an amplification of fluctuations in heading in the group, which can trigger U-turns. These collective U-turns are mostly initiated by individuals at the front of the group. Once an individual has initiated a U-turn, the new direction propagates through the group from front to back without amplification or dampening, resembling the dynamics of falling dominoes. The mean time between collective U-turns sharply increases as the size of the group increases. We develop an Ising spin model integrating anisotropic and asymmetrical interactions between fish and their tendency to follow the majority of their neighbours nonlinearly (social conformity). The model quantitatively reproduces key features of the dynamics and the frequency of collective U-turns observed in experiments.

Physics-based simulations of aerial attacks by peregrine falcons reveal that stooping at high speed maximizes catch success against agile prey.

The peregrine falcon Falco peregrinus is renowned for attacking its prey from high altitude in a fast controlled dive called a stoop. Many other raptors employ a similar mode of attack, but the functional benefits of stooping remain obscure. Here we investigate whether, when, and why stooping promotes catch success, using a three-dimensional, agent-based modeling approach to simulate attacks of falcons on aerial prey. We simulate avian flapping and gliding flight using an analytical quasi-steady model of the aerodynamic forces and moments, parametrized by empirical measurements of flight morphology. The model-birds' flight control inputs are commanded by their guidance system, comprising a phenomenological model of its vision, guidance, and control. To intercept its prey, model-falcons use the same guidance law as missiles (pure proportional navigation); this assumption is corroborated by empirical data on peregrine falcons hunting lures. We parametrically vary the falcon's starting position relative to its prey, together with the feedback gain of its guidance loop, under differing assumptions regarding its errors and delay in vision and control, and for three different patterns of prey motion. We find that, when the prey maneuvers erratically, high-altitude stoops increase catch success compared to low-altitude attacks, but only if the falcon's guidance law is appropriately tuned, and only given a high degree of precision in vision and control. Remarkably, the optimal tuning of the guidance law in our simulations coincides closely with what has been observed empirically in peregrines. High-altitude stoops are shown to be beneficial because their high airspeed enables production of higher aerodynamic forces for maneuvering, and facilitates higher roll agility as the wings are tucked, each of which is essential to catching maneuvering prey at realistic response delays.

The confusion effect when attacking simulated three-dimensional starling flocks.

The confusion effect describes the phenomenon of decreasing predator attack success with increasing prey group size. However, there is a paucity of research into the influence of this effect in coherent groups, such as flocks of European starlings (Sturnus vulgaris). Here, for the first time, we use a computer game style experiment to investigate the confusion effect in three dimensions. To date, computerized studies on the confusion effect have used two-dimensional simulations with simplistic prey movement and dynamics. Our experiment is the first investigation of the effects of flock size and density on the ability of a (human) predator to track and capture a target starling in a realistically simulated three-dimensional flock of starlings. In line with the predictions of the confusion effect, modelled starlings appear to be safer from predation in larger and denser flocks. This finding lends credence to previous suggestions that starling flocks have anti-predator benefits and, more generally, it suggests that active increases in density in animal groups in response to predation may increase the effectiveness of the confusion effect.

"Targeting or supporting, what drives patterns of aggressive intervention in fights?".

GrooFiWorld is an individual-based, computational model of social interactions that can be used to examine factors underlying reciprocation and interchange of social behavior in primate societies. Individuals within GrooFiWorld are programed to maintain spatial proximity and thereby form a group. When an individual encounters another individual in its proximity, the individual attacks the other if the risk of losing is low. Otherwise, the individual considers grooming the other. Patterns of social behavior that emerge in the model resemble empirical data from primates. Triadic aggression emerges when an individual attacks one of the former combatants by chance immediately after an aggressive interaction, and reciprocation and interchange of grooming and support emerge even though individuals have no intention to help others or pay back services. The model generates predictions for patterns of contra-intervention that are counterintuitive within a framework of interchange of social services, such as that individuals receive more contra-intervention from those whom they groom more frequently. Here we tested these predictions in data collected on social interactions in a group of bonnet macaques (Macaca radiata). We confirmed the predictions of the model in the sense that contra-intervention was strongly correlated with dyadic aggression which suggests that contra-intervention is a subset of dyadic aggression. Adult females directed more contra-intervention to those individuals from whom they received more grooming. Further, contra-intervention was directed down the dominance hierarchy such that adult females received more contra-intervention from higher ranking females. Because these findings are consistent with the predictions from the GrooFiWorld model, they suggest that the distribution of interventions in fights is regulated by factors such as dominance rank and spatial structure rather than a motivation to help others and interchange social services.

Early maternal loss affects social integration of chimpanzees throughout their lifetime.

The long-term effects of early adverse experiences on later psychosocial functioning are well described in humans, but sparsely documented for chimpanzees. In our earlier studies, we investigated the effects of maternal and social deprivation on three groups of ex-laboratory chimpanzees who experienced either an early or later onset of long-term deprivation. Here we expand our research by adding data on subjects that came from two stable zoo groups. The groups comprised of early maternally deprived wild-caught chimpanzees and non-deprived zoo-born chimpanzees. We found that compared to zoo chimpanzees, ex-laboratory chimpanzees were more restricted regarding their association partners in the newly formed groups, but not during their second year of group-life, indicating that social stability has an important influence on the toleration of association partners close-by. Social grooming activity, however, was impaired in early long-term deprived ex-laboratory chimpanzees as well as in early maternally deprived zoo chimpanzees compared to non-deprived zoo chimpanzees. Thus, we conclude that early maternal loss has lifelong effects on the social integration of chimpanzees which becomes evident in their grooming networks. Although the retrospective nature of our study prevents a clear causal explanation, our results are of importance for understanding the development of social competence in chimpanzees.

What underlies waves of agitation in starling flocks.

Fast transfer of information in groups can have survival value. An example is the so-called wave of agitation observed in groups of animals of several taxa under attack. It has been shown to reduce predator success. It usually involves the repetition of a manoeuvre throughout the group, transmitting the information of the attack quickly, faster than the group moves itself. The specific manoeuvre underlying a wave is typically known, but not so in starlings (Sturnus vulgaris). Although waves of agitation in starling flocks have been suggested to reflect density waves, exact escape manoeuvres cannot be distinguished because flocks are spatially too far away. Therefore, waves may also reflect orientation waves (due to escape by rolling). In the present study, we investigate this issue in a computational model, StarDisplay. We use this model because its flocks have been shown to resemble starling flocks in many traits. In the model, we show that agitation waves result from changes in orientation rather than in density. They resemble empirical data both qualitatively in visual appearance and quantitatively in wave speed. In the model, local interactions with only two to seven closest neighbours suffice to generate empirical wave speed. Wave speed increases with the number of neighbours mimicked or repeated from and the distance to them. It decreases with reaction time and with time to identify the escape manoeuvre of others and is not affected by flock size. Our findings can be used as predictions for empirical studies.

Diffusion and topological neighbours in flocks of starlings: relating a model to empirical data.

Moving in a group while avoiding collisions with group members causes internal dynamics in the group. Although these dynamics have recently been measured quantitatively in starling flocks (Sturnus vulgaris), it is unknown what causes them. Computational models have shown that collective motion in groups is likely due to attraction, avoidance and, possibly, alignment among group members. Empirical studies show that starlings adjust their movement to a fixed number of closest neighbours or topological range, namely 6 or 7 and assume that each of the three activities is done with the same number of neighbours (topological range). Here, we start from the hypothesis that escape behavior is more effective at preventing collisions in a flock when avoiding the single closest neighbor than compromising by avoiding 6 or 7 of them. For alignment and attraction, we keep to the empirical topological range. We investigate how avoiding one or several neighbours affects the internal dynamics of flocks of starlings in our computational model StarDisplay. By comparing to empirical data, we confirm that internal dynamics resemble empirical data more closely if flock members avoid merely their single, closest neighbor. Our model shows that considering a different number of interaction partners per activity represents a useful perspective and that changing a single parameter, namely the number of interaction partners that are avoided, has several effects through selforganisation.

The evolution of different forms of sociality: behavioral mechanisms and eco-evolutionary feedback.

Different forms of sociality have evolved via unique evolutionary trajectories. However, it remains unknown to what extent trajectories of social evolution depend on the specific characteristics of different species. Our approach to studying such trajectories is to use evolutionary case-studies, so that we can investigate how grouping co-evolves with a multitude of individual characteristics. Here we focus on anti-predator vigilance and foraging. We use an individual-based model, where behavioral mechanisms are specified, and costs and benefits are not predefined. We show that evolutionary changes in grouping alter selection pressures on vigilance, and vice versa. This eco-evolutionary feedback generates an evolutionary progression from "leader-follower" societies to "fission-fusion" societies, where cooperative vigilance in groups is maintained via a balance between within- and between-group selection. Group-level selection is generated from an assortment that arises spontaneously when vigilant and non-vigilant foragers have different grouping tendencies. The evolutionary maintenance of small groups, and cooperative vigilance in those groups, is therefore achieved simultaneously. The evolutionary phases, and the transitions between them, depend strongly on behavioral mechanisms. Thus, integrating behavioral mechanisms and eco-evolutionary feedback is critical for understanding what kinds of intermediate stages are involved during the evolution of particular forms of sociality.

A novel mechanism for a survival advantage of vigilant individuals in groups.

In many animal species, vigilance is crucial for avoiding predation. In groups, however, nonvigilant individuals could benefit from the vigilance of others without any of the associated costs. In an evolutionary sense, such exploitation may be compensated if vigilant individuals have a survival advantage. The novelty in our model is that the probability to detect a predator is "distance dependent." We show that even if nonvigilant individuals benefit fully from information produced by vigilant individuals, vigilant individuals nevertheless enjoy a survival advantage. This happens because detection of predators is more likely when vigilant individuals happen to be targets of predation. We expect this distance-dependent mechanism to be compatible with previously reported mechanisms.