Influence of behavioural and morphological group composition on pigeon flocking dynamics.

Animals rely on movement to explore and exploit resources in their environment. While movement can provide energetic benefits, it also comes with energetic costs. This study examines how group phenotypic composition influences individual speed and energy expenditure during group travel in homing pigeons. We manipulated the composition of pigeon groups based on body mass and leadership rank. Our findings indicate that groups of 'leader' phenotypes show faster speeds and greater cohesion than 'follower' phenotype groups. Additionally, we show that groups of homogenous mass composition, whether all heavy or all light, were faster and expended less energy over the course of a whole flight than flocks composed of a mixture of heavy and light individuals. We highlight the importance of considering individual-level variation in social-level studies, and the interaction between individual and group-level traits in governing speed and the costs of travel.

'Selfish herders' finish last in mobile animal groups.

Predation is a powerful selective pressure and probably a driver of why many animal species live in groups. One key explanation for the evolution of sociality is the 'selfish herd' model, which describes how individuals who stay close to others effectively put neighbours between themselves and a predator to survive incoming attacks. This model is often illustrated with reference to herds of ungulates, schools of fish or flocks of birds. Yet in nature, when a predator strikes, herds are often found fleeing cohesively in the same direction, not jostling for position in the centre of the group. This paper highlights a critical assumption of the original model, namely that prey do not move in response to position of their predator. In this model, I relax this assumption and find that individuals who adopt 'selfish herd' behaviour are often more likely to be captured, because they end up at the back of a fleeing herd. By contrast, individuals that adopt a rule of 'neighbour to neighbour alignment' are able to avoid rearmost positions in a moving herd. Alignment is more successful than selfish herding across much of the parameter space, which may explain why highly aligned fleeing behaviour is commonly observed in nature.

Pigeon leadership hierarchies are not dependent on environmental contexts or individual phenotypes.

Remaining cohesive on the move can be beneficial for animal groups. As such, animal groups have evolved coordination mechanisms such as leadership to resolve navigational conflicts of interest. Consistent "leaders" may have an intrinsic advantage over "followers" which compromise on their preferred route to retain cohesion, which highlights the question of the inter-individual variation (phenotype) that can predict leadership. Studies in both birds and fish have revealed that intrinsically faster individuals can lead movements, and leading movements propagate from the front edge of the flock/shoal. However, these experiments are generally conducted in relatively "familiar" environments, where the degree of compromise between the "leaders" and "followers" is low. We suggested that inter-individual differences in route efficiency, while not explanatory of leadership from familiar locations, may emerge as predictors of leadership from unfamiliar locations. We tested this prediction - and the potential impact of multiple other behavioral, morphological and "in-flight" phenotypes on leadership - using two groups of homing pigeons (Columba livia) (N = 16), a classic model species of leadership. We recorded N = 966 unique GPS trajectories from birds in (i) solo and familiar, and (ii) solo and unfamiliar contexts to measure solo speed and solo route efficiency; and (iii) group and familiar, and (iv) group and unfamiliar contexts to assess group leadership. Pigeon leadership hierarchies were similar across environmental context (i.e., familiarity). However, we found that no covariates could consistently predict leadership score in either context.

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.

Artificial mass loading disrupts stable social order in pigeon dominance hierarchies.

Dominance hierarchies confer benefits to group members by decreasing the incidences of physical conflict, but may result in certain lower ranked individuals consistently missing out on access to resources. Here, we report a linear dominance hierarchy remaining stable over time in a closed population of birds. We show that this stability can be disrupted, however, by the artificial mass loading of birds that typically comprise the bottom 50% of the hierarchy. Mass loading causes these low-ranked birds to immediately become more aggressive and rise-up the dominance hierarchy; however, this effect was only evident in males and was absent in females. Removal of the artificial mass causes the hierarchy to return to its previous structure. This interruption of a stable hierarchy implies a strong direct link between body mass and social behaviour and suggests that an individual's personality can be altered by the artificial manipulation of body mass.

When flocking is costly: reduced cluster-flock density over long-duration flight in pigeons.

Birds which fly in coordinated cluster-flocks can benefit through the formation of group-level structures and patterns which can deter predators by visual confusion. Though unlike V-formation flight, cluster-flocking increases the energetic cost of flight, particularly in denser flocks. Cluster formations therefore provide a unique opportunity to investigate trade-offs between increased work rate (e.g. higher flap frequency) and other benefits of flocking. As part of a routine 9-km training flight release, a flock of six homing pigeons (Columba livia) with 5 Hz GPS and 200 Hz accelerometer biologgers attached flew an alternative trajectory totalling 177 km and 256 min of flight. We provide the first evidence that during a long-duration flight, pigeons' pairwise and group-level distances increased (i.e. group structure changed), while flap frequency decreased over time. This implies that as birds tire during long-duration flight, the ultimate functions of cluster-flocking-primarily anti-predator benefits-are overridden by the proximate costs of flying close to conspecifics.