Initiation and spread of escape waves within animal groups

The exceptional reactivity of animal collectives to predatory attacks is thought to be due to rapid, but local, transfer of information between group members. These groups turn together in unison and produce escape waves. However, it is not clear how escape waves are created from local interactions, nor is it understood how these patterns are shaped by natural selection. By startling schools of fish with a simulated attack in an experimental arena, we demonstrate that changes in the direction and speed by a small percentage of individuals that detect the danger initiate an escape wave. This escape wave consists of a densely packed band of individuals that causes other school members to change direction. In the majority of cases this wave passes through the entire group. We use a simulation model to demonstrate that this mechanism can, through local interactions alone, produce arbitrarily large escape waves. In the model, when we set the group density to that seen in real fish schools, we find that the risk to the members at the edge of the group is roughly equal to the risk of those within the group. Our experiments and modelling results provide a plausible explanation for how escape waves propagate in Nature without centralised control

Escape path complexity and its context dependency in Pacific blue-eyes (Pseudomugil signifer)

The escape trajectories animals take following a predatory attack appear to show high degrees of apparent 'randomness' - a property that has been described as 'protean behaviour'. Here we present a method of quantifying the escape trajectories of individual animals using a path complexity approach. When fish (Pseudomugil signifer) were attacked either on their own or in groups, we find that an individual's path rapidly increases in entropy (our measure of complexity) following the attack. For individuals on their own, this entropy remains elevated (indicating a more random path) for a sustained period (10 seconds) after the attack, whilst it falls more quickly for individuals in groups. The entropy of the path is context dependent. When attacks towards single fish come from greater distances, a fish's path shows less complexity compared to attacks that come from short range. This context dependency effect did not exist, however, when individuals were in groups. Nor did the path complexity of individuals in groups depend on a fish's local density of neighbours. We separate out the components of speed and direction changes to determine which of these components contributes to the overall increase in path complexity following an attack. We found that both speed and direction measures contribute similarly to an individual's path's complexity in absolute terms. Our work highlights the adaptive behavioural tactics that animals use to avoid predators and also provides a novel method for quantifying the escape trajectories of animals.Comment: 9 page

Predators attacking virtual prey reveal the costs and benefits of leadership.

A long-standing assumption in social behavior is that leadership incurs costs as well as benefits, and this tradeoff can result in diversified social roles in groups. The major cost of leadership in moving animal groups is assumed to be predation, with individuals leading from the front of groups being targeted more often by predators. Nevertheless, empirical evidence for this is limited, and experimental tests are entirely lacking. To avoid confounding effects associated with observational studies, we presented a simulation of virtual prey to real fish predators to directly assess the predation cost of leadership. Prey leading others are at greater risk than those in the middle of groups, confirming that any benefits of leading may be offset by predation costs. Importantly, however, followers confer a net safety benefit to leaders, as prey leading others were less likely to be attacked compared with solitary prey. We also find that the predators preferentially attacked when solitary individuals were more frequent, but this effect was relatively weak compared with the preference for attacking solitary prey during an attack. Using virtual prey, where the appearance and behavior of the prey can be manipulated and controlled exactly, we reveal a hierarchy of risk from solitary to leading to following social strategies. Our results suggest that goal-orientated individuals (i.e., potential leaders) are under selective pressure to maintain group cohesion, favoring effective leadership rather than group fragmentation. Our results have significant implications for understanding the evolution and maintenance of different social roles in groups.his work was supported by Natural Environment Research Council Independent Research Fellowship NE/K009370/1 and Leverhulme Trust Grant RPG-2017-041 V (to C.C.I.)

Quantifying the structure and dynamics of fish shoals under predation threat in three dimensions

Detailed quantifications of how predators and their grouping prey interact in three dimensions (3D) remain rare. Here we record the structure and dynamics of fish shoals (Pseudomugil signifer) in 3D both with and without live predators (Philypnodon grandiceps) under controlled laboratory conditions. Shoals adopted two distinct types of shoal structure; 'sphere-like' geometries at depth, and flat 'carpet-like' structures at the water's surface, with shoals becoming more compact in both horizontal and vertical planes in the presence of a predator. The predators actively stalked and at- tacked the prey, with attacks being initiated when the shoals were not in their usual configurations. These attacks caused the shoals to break apart, but shoal reformation was rapid, and involved individuals adjusting their positions in both horizontal and vertical dimensions. Our analyses revealed that targeted prey were more isolated from other conspecifics, and were closer in terms of distance and direction to the predator compared to non-targeted prey. Moreover, which prey were targeted could largely be identified based on individuals' positions from a single plane. This highlights that previously proposed 2D theoretical models and their assumptions appear valid when considering how predators target groups in 3D. Our work provides experimental, and not just anecdotal, sup- port for classic theoretical predictions, and also lends new insights into predatory-prey interactions in three-dimensional environments

Local interactions and global properties of wild, free-ranging stickleback shoals

Funding: Australian Research Council. A.J.W.W. and T.M.S. were supported by a Discovery Project Grant from the Australian Research Council. D.J.T.S. and J.E.H.-R. were supported by a Knut & Alice Wallenberg Foundation Grant.Collective motion describes the global properties of moving groups of animals and the self-organized, coordinated patterns of individual behaviour that produce them. We examined the group-level patterns and local interactions between individuals in wild, free-ranging shoals of three-spine sticklebacks, Gasterosteus aculeatus. Our data reveal that the highest frequencies of near-neighbour encounters occur at between one and two body lengths from a focal fish, with the peak frequency alongside a focal individual. Fish also show the highest alignment with these laterally placed individuals, and generally with animals in front of themselves. Furthermore, fish are more closely matched in size, speed and orientation to their near neighbours than to more distant neighbours, indicating local organization within groups. Among the group level properties reported here, we find that polarization is strongly influenced by group speed, but also the variation in speed among individuals and the nearest neighbour distances of group members. While we find no relationship between group order and group size, we do find that larger groups tend to have lower nearest neighbour distances, which in turn may be important in maintaining group order.Publisher PDFPeer reviewe

Anthropogenic noise pollution from pile-driving disrupts the structure and dynamics of fish shoals

Noise produced from a variety of human activities can affect the physiology and behaviour of individual animals, but whether noise disrupts the social behaviour of animals is largely unknown. Animal groups such as flocks of birds or shoals of fish use simple interaction rules to coordinate their movements with near neighbours. In turn, this coordination allows individuals to gain the benefits of group living such as reduced predation risk and social information exchange. Noise could change how individuals interact in groups if noise is perceived as a threat, or if it masked, distracted or stressed individuals, and this could have impacts on the benefits of grouping. Here, we recorded trajectories of individual juvenile seabass (<i>Dicentrarchus labrax</i>) in groups under controlled laboratory conditions. Groups were exposed to playbacks of either ambient background sound recorded in their natural habitat, or playbacks of pile-driving, commonly used in marine construction. The pile-driving playback affected the structure and dynamics of the fish shoals significantly more than the ambient-sound playback. Compared to the ambient-sound playback, groups experiencing the pile-driving playback became less cohesive, less directionally ordered, and were less correlated in speed and directional changes. In effect, the additional-noise treatment disrupted the abilities of individuals to coordinate their movements with one another. Our work highlights the potential for noise pollution from pile-driving to disrupt the collective dynamics of fish shoals, which could have implications for the functional benefits of groups' collective behaviour

Context-dependent lateralized feeding strategies in blue whales.

Lateralized behaviors benefit individuals by increasing task efficiency in foraging and anti-predator behaviors [1-4]. The conventional lateralization paradigm suggests individuals are left or right lateralized, although the direction of this laterality can vary for different tasks (e.g. foraging or predator inspection/avoidance). By fitting tri-axial movement sensors to blue whales (Balaenoptera musculus), and by recording the direction and size of their rolls during lunge feeding events, we show how these animals differ from such a paradigm. The strength and direction of individuals' lateralization were related to where and how the whales were feeding in the water column. Smaller rolls (≤180°) predominantly occurred at depth (>70 m), with whales being more likely to rotate clockwise around their longest axis (right lateralized). Larger rolls (>180°), conversely, occurred more often at shallower depths (<70 m) and were more likely to be performed anti-clockwise (left lateralized). More acrobatic rolls are typically used to target small, less dense krill patches near the water's surface [5,6], and we posit that the specialization of lateralized feeding strategies may enhance foraging efficiency in environments with heterogeneous prey distributions

Body size affects the strength of social interactions and spatial organization of a schooling fish (Pseudomugil signifer)

While a rich variety of self-propelled particle models propose to explain the collective motion of fish and other animals, rigorous statistical comparison between models and data remains a challenge. Plausible models should be flexible enough to capture changes in the collective behaviour of animal groups at their different developmental stages and group sizes. Here, we analyse the statistical properties of schooling fish (Pseudomugil signifer) through a combination of experiments and simulations. We make novel use of a Boltzmann inversion method, usually applied in molecular dynamics, to identify the effective potential of the mean force of fish interactions. Specifically, we show that larger fish have a larger repulsion zone, but stronger attraction, resulting in greater alignment in their collective motion. We model the collective dynamics of schools using a self-propelled particle model, modified to include varying particle speed and a local repulsion rule. We demonstrate that the statistical properties of the fish schools are reproduced by our model, thereby capturing a number of features of the behaviour and development of schooling fish