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 attacked 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, support for classic theoretical predictions and also lends new insights into predatory–prey interactions in three-dimensional environments.
We use computer simulations to study the onset of collective motion in systems of interacting active particles. Our model is a swarm of active Brownian particles with an internal energy depot and interactions inspired by the dissipative particle dynamics method, imposing pairwise friction force on the nearest neighbors. We study orientational ordering in a 2D system as a function of energy influx rate and particle density. The model demonstrates a transition into the ordered state on increasing the particle density and increasing the input power. Although both the alignment mechanism and the character of individual motion in our model differ from those in the well-studied Vicsek model, it demonstrates identical statistical properties and phase behavior.
We study dynamic self-organisation and order-disorder transitions in a two-dimensional system of self-propelled particles. Our model is a variation of the Vicsek model, where particles align the motion to their neighbours but repel each other at short distances. We use computer simulations to measure the orientational order parameter for particle velocities as a function of intensity of internal noise or particle density. We show that in addition to the transition to an ordered state on increasing the particle density, as reported previously, there exists a transition into a disordered phase at the higher densities, which can be attributed to the destructive action of the repulsions. We demonstrate that the transition into the ordered phase is accompanied by the onset of algebraic behaviour of the two-point velocity correlation function and by a non-monotonous variation of the velocity relaxation time. The critical exponent for the decay of the velocity correlation function in the ordered phase depends on particle concentration at low densities but assumes a universal value in more dense systems.
Collective motion occurs when individuals use social interaction rules to respond to the movements and positions of their neighbors. How readily these social decisions are shaped by selection remains unknown. Through artificial selection on fish (guppies, Poecilia reticulata) for increased group polarization, we demonstrate rapid evolution in how individuals use social interaction rules. Within only three generations, groups of polarization-selected females showed a 15% increase in polarization, coupled with increased cohesiveness, compared to fish from control lines. Although lines did not differ in their physical swimming ability or exploratory behavior, polarization-selected fish adopted faster speeds, particularly in social contexts, and showed stronger alignment and attraction responses to multiple neighbors. Our results reveal the social interaction rules that change when collective behavior evolves.
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.
A widespread problem in biological research is assessing whether a model adequately describes some real-world data. But even if a model captures the large-scale statistical properties of the data, should we be satisfied with it? We developed a method, inspired by Alan Turing, to assess the effectiveness of model fitting. We first built a self-propelled particle model whose properties (order and cohesion) statistically matched those of real fish schools. We then asked members of the public to play an online game (a modified Turing test) in which they attempted to distinguish between the movements of real fish schools or those generated by the model. Even though the statistical properties of the real data and the model were consistent with each other, the public could still distinguish between the two, highlighting the need for model refinement. Our results demonstrate that we can use ‘citizen science’ to cross-validate and improve model fitting not only in the field of collective behaviour, but also across a broad range of biological systems.
Animals living in groups can show substantial variation in social traits and this affects their social organisation. However, as the specific mechanisms driving this organisation are difficult to identify in already-organised groups typically found in the wild, the contribution of inter-individual variation to grouplevel behaviour remains enigmatic. Here, we present results of an experiment to create and compare groups that vary in social organisation, and study how individual behaviour varies between these groups. We iteratively sorted individuals between groups of guppies (Poecilia reticulata) by ranking the groups according to their directional alignment and then mixing similar groups. Over the rounds of sorting the consistency of the group rankings increased, producing groups that varied significantly in key social behaviours such as collective activity and group cohesion. The repeatability of the underlying individual behaviour was then estimated by comparing the experimental data to simulations. At the level of basic locomotion, individuals in more coordinated groups displayed stronger interactions with the centre of the group, and weaker interactions with their nearest neighbours. We propose that this provides the basis for a passive phenotypic assortment mechanism that may explain the structures of social networks in the wild.
For most animals, feeding includes two behaviors: foraging to find a food patch and food intake once a patch is found. The nematode Caenorhabditis elegans is a useful model for studying the genetics of both behaviors. However, most methods of measuring feeding in worms quantify either foraging behavior or food intake, but not both. Imaging the depletion of fluorescently labeled bacteria provides information on both the distribution and amount of consumption, but even after patch exhaustion a prominent background signal remains, which complicates quantification. Here, we used a bioluminescent Escherichia coli strain to quantify C. elegans feeding. With light emission tightly coupled to active metabolism, only living bacteria are capable of bioluminescence, so the signal is lost upon ingestion. We quantified the loss of bioluminescence using N2 reference worms and eat-2 mutants, and found a nearly 100-fold increase in signal-to-background ratio and lower background compared to loss of fluorescence. We also quantified feeding using aggregating npr-1 mutant worms. We found that groups of npr-1 mutants first clear bacteria from within the cluster before foraging collectively for more food; similarly, during large population swarming, only worms at the migrating front are in contact with bacteria. These results demonstrate the usefulness of bioluminescent bacteria for quantifying feeding and generating insights into the spatial pattern of food consumption.
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