Characterization of lab-based swarms of Anopheles gambiae mosquitoes using 3D-video tracking.

Mosquito copulation is a crucial determinant of its capacity to transmit malaria-causing Plasmodium parasites as well as underpinning several highly-anticipated vector control methodologies such as gene drive and sterile insect technique. For the anopheline mosquitoes responsible for African malaria transmission, mating takes place within crepuscular male swarms which females enter solely to mate. However, the mechanisms that regulate swarm structure or that govern mate choice remain opaque. We used 3D-video tracking approaches and computer vision algorithms developed for the study of other complex biological systems to document swarming behavior of a lab-adapted Anopheles gambiae line in a lab-based setting. By reconstructing trajectories of individual mosquitoes lasting up to 15.88 s, in swarms containing upwards of 200 participants, we documented swarm-like behavior in both males and females. In single sex swarms, encounters between individuals were fleeting (< 0.75 s). By contrast, in mixed swarms, we were able to detect 79 'brief encounters' (> 0.75 s; < 2.5 s) and 17 longer-lived encounters (> 2.5 s). We also documented several examples of apparent male-male mating competition. These findings represent the first steps towards a more detailed and quantitative description of swarming and courtship behavior in one of the most important vectors of malaria.

Renormalization group study of marginal ferromagnetism.

When studying the collective motion of biological groups, a useful theoretical framework is that of ferromagnetic systems, in which the alignment interactions are a surrogate of the effective imitation among the individuals. In this context, the experimental discovery of scale-free correlations of speed fluctuations in starling flocks poses a challenge to common statistical physics wisdom, as in the ordered phase of standard ferromagnetic models with O(n) symmetry, the modulus of the order parameter has finite correlation length. To make sense of this anomaly, a ferromagnetic theory has been proposed, where the bare confining potential has zero second derivative (i.e., it is marginal) along the modulus of the order parameter. The marginal model exhibits a zero-temperature critical point, where the modulus correlation length diverges, hence allowing us to boost both correlation and collective order by simply reducing the temperature. Here, we derive an effective field theory describing the marginal model close to the T=0 critical point and calculate the renormalization group equations at one loop within a momentum shell approach. We discover a nontrivial scenario, as the cubic and quartic vertices do not vanish in the infrared limit, while the coupling constants effectively regulating the exponents ν and η have upper critical dimension d_{c}=2, so in three dimensions the critical exponents acquire their free values, ν=1/2 and η=0. This theoretical scenario is verified by a Monte Carlo study of the modulus susceptibility in three dimensions, where the standard finite-size scaling relations have to be adapted to the case of d>d_{c}. The numerical data fully confirm our theoretical results.

Marginal speed confinement resolves the conflict between correlation and control in collective behaviour.

Speed fluctuations of individual birds in natural flocks are moderate, due to the aerodynamic and biomechanical constraints of flight. Yet the spatial correlations of such fluctuations are scale-free, namely they have a range as wide as the entire group, a property linked to the capacity of the system to collectively respond to external perturbations. Scale-free correlations and moderate fluctuations set conflicting constraints on the mechanism controlling the speed of each agent, as the factors boosting correlation amplify fluctuations, and vice versa. Here, using a statistical field theory approach, we suggest that a marginal speed confinement that ignores small deviations from the natural reference value while ferociously suppressing larger speed fluctuations, is able to reconcile scale-free correlations with biologically acceptable group's speed. We validate our theoretical predictions by comparing them with field experimental data on starling flocks with group sizes spanning an unprecedented interval of over two orders of magnitude.

Dynamical Renormalization Group for Mode-Coupling Field Theories with Solenoidal Constraint.

The recent inflow of empirical data about the collective behaviour of strongly correlated biological systems has brought field theory and the renormalization group into the biophysical arena. Experiments on bird flocks and insect swarms show that social forces act on the particles' velocity through the generator of its rotations, namely the spin, indicating that mode-coupling field theories are necessary to reproduce the correct dynamical behaviour. Unfortunately, a theory for three coupled fields-density, velocity and spin-has a prohibitive degree of intricacy. A simplifying path consists in getting rid of density fluctuations by studying incompressible systems. This requires imposing a solenoidal constraint on the primary field, an unsolved problem even for equilibrium mode-coupling theories. Here, we perform an equilibrium dynamic renormalization group analysis of a mode-coupling field theory subject to a solenoidal constraint; using the classification of Halperin and Hohenberg, we can dub this case as a solenoidal Model G. We demonstrate that the constraint produces a new vertex that mixes static and dynamical coupling constants, and that this vertex is essential to grant the closure of the renormalization group structure and the consistency of dynamics with statics. Interestingly, although the solenoidal constraint leads to a modification of the static universality class, we find that it does not change the dynamical universality class, a result that seems to represent an exception to the general rule that dynamical universality classes are narrower than static ones. Our results constitute a solid stepping stone in the admittedly large chasm towards developing an off-equilibrium mode-coupling theory of biological groups.

SpaRTA Tracking Across Occlusions via Partitioning of 3D Clouds of Points.

Any 3D tracking algorithm has to deal with occlusions: multiple targets get so close to each other that the loss of their identities becomes likely; hence, potentially affecting the very quality of the data with interrupted trajectories and identity switches. Here, we present a novel tracking method that addresses the problem of occlusions within large groups of featureless objects by means of three steps: i) it represents each target as a cloud of points in 3D; ii) once a 3D cluster corresponding to an occlusion occurs, it defines a partitioning problem by introducing a cost function that uses both attractive and repulsive spatio-temporal proximity links; and iii) it minimizes the cost function through a semi-definite optimization technique specifically designed to cope with the presence of multi-minima landscapes. The algorithm is designed to work on 3D data regardless of the experimental method used: multicamera systems, lidars, radars, and RGB-D systems. By performing tests on public data-sets, we show that the new algorithm produces a significant improvement over the state-of-the-art tracking methods, both by reducing the number of identity switches and by increasing the accuracy of the estimated positions of the targets in real space.

Renormalization group crossover in the critical dynamics of field theories with mode coupling terms.

Motivated by the collective behavior of biological swarms, we study the critical dynamics of field theories with coupling between order parameter and conjugate momentum in the presence of dissipation. Under a fixed-network approximation, we perform a dynamical renormalization group calculation at one loop in the near-critical disordered region, and we show that the violation of momentum conservation generates a crossover between an unstable fixed point, characterized by a dynamic critical exponent z=d/2, and a stable fixed point with z=2. Interestingly, the two fixed points have different upper critical dimensions. The interplay between these two fixed points gives rise to a crossover in the critical dynamics of the system, characterized by a crossover exponent κ=4/d. The crossover is regulated by a conservation length scale R_{0}, given by the ratio between the transport coefficient and the effective friction, which is larger as the dissipation is smaller: Beyond R_{0}, the stable fixed point dominates, while at shorter distances dynamics is ruled by the unstable fixed point and critical exponent, a behavior which is all the more relevant in finite-size systems with weak dissipation. We run numerical simulations in three dimensions and find a crossover between the exponents z=3/2 and z=2 in the critical slowdown of the system, confirming the renormalization group results. From the biophysical point of view, our calculation indicates that in finite-size biological groups mode coupling terms in the equation of motion can significantly change the dynamical critical exponents even in the presence of dissipation, a step toward reconciling theory with experiments in natural swarms. Moreover, our result provides the scale within which fully conservative Bose-Einstein condensation is a good approximation in systems with weak symmetry-breaking terms violating number conservation, as quantum magnets or photon gases.

Dynamical Renormalization Group Approach to the Collective Behavior of Swarms.

We study the critical behavior of a model with nondissipative couplings aimed at describing the collective behavior of natural swarms, using the dynamical renormalization group under a fixed-network approximation. At one loop, we find a crossover between an unstable fixed point, characterized by a dynamical critical exponent z=d/2, and a stable fixed point with z=2, a result we confirm through numerical simulations. The crossover is regulated by a length scale given by the ratio between the transport coefficient and the effective friction, so that in finite-size biological systems with low dissipation, dynamics is ruled by the unstable fixed point. In three dimensions this mechanism gives z=3/2, a value significantly closer to the experimental window, 1.0≤z≤1.3, than the value z≈2 numerically found in fully dissipative models, either at or off equilibrium. This result indicates that nondissipative dynamical couplings are necessary to develop a theory of natural swarms fully consistent with experiments.

Nonsymmetric Interactions Trigger Collective Swings in Globally Ordered Systems.

Many systems in nature, from ferromagnets to flocks of birds, exhibit ordering phenomena on the large scale. In condensed matter systems, order is statistically robust for large enough dimensions, with relative fluctuations due to noise vanishing with system size. Several biological systems, however, are less stable and spontaneously change their global state on relatively short time scales. Here we show that there are two crucial ingredients in these systems that enhance the effect of noise, leading to collective changes of state on finite time scales and off-equilibrium behavior: the nonsymmetric nature of interactions between individuals, and the presence of local heterogeneities in the topology of the network. Our results might explain what is observed in several living systems and are consistent with recent experimental data on bird flocks and other animal groups.

Local equilibrium in bird flocks.

The correlated motion of flocks is an instance of global order emerging from local interactions. An essential difference with analogous ferromagnetic systems is that flocks are active: animals move relative to each other, dynamically rearranging their interaction network. The effect of this off-equilibrium element is well studied theoretically, but its impact on actual biological groups deserves more experimental attention. Here, we introduce a novel dynamical inference technique, based on the principle of maximum entropy, which accodomates network rearrangements and overcomes the problem of slow experimental sampling rates. We use this method to infer the strength and range of alignment forces from data of starling flocks. We find that local bird alignment happens on a much faster timescale than neighbour rearrangement. Accordingly, equilibrium inference, which assumes a fixed interaction network, gives results consistent with dynamical inference. We conclude that bird orientations are in a state of local quasi-equilibrium over the interaction length scale, providing firm ground for the applicability of statistical physics in certain active systems.

Spatio-temporal correlations in models of collective motion ruled by different dynamical laws.

Information transfer is an essential factor in determining the robustness of biological systems with distributed control. The most direct way to study the mechanisms ruling information transfer is to experimentally observe the propagation across the system of a signal triggered by some perturbation. However, this method may be inefficient for experiments in the field, as the possibilities to perturb the system are limited and empirical observations must rely on natural events. An alternative approach is to use spatio-temporal correlations to probe the information transfer mechanism directly from the spontaneous fluctuations of the system, without the need to have an actual propagating signal on record. Here we test this method on models of collective behaviour in their deeply ordered phase by using ground truth data provided by numerical simulations in three dimensions. We compare two models characterized by very different dynamical equations and information transfer mechanisms: the classic Vicsek model, describing an overdamped noninertial dynamics and the inertial spin model, characterized by an underdamped inertial dynamics. By using dynamic finite-size scaling, we show that spatio-temporal correlations are able to distinguish unambiguously the diffusive information transfer mechanism of the Vicsek model from the linear mechanism of the inertial spin model.

Entropic effects in a nonequilibrium system: Flocks of birds.

When European starlings come together to form a flock, the distribution of their individual velocities narrows around the mean velocity of the flock. We argue that, in a broad class of models for the joint distribution of positions and velocities, this narrowing generates an entropic effect that opposes the cohesion of the flock. The strength of this effect depends strongly on the nature of the interactions among birds: If birds are coupled to a fixed number of neighbors, the entropic forces are weak, while if they couple to all other birds within a fixed distance, the entropic effects are sufficient to tear a flock apart.

GReTA-A Novel Global and Recursive Tracking Algorithm in Three Dimensions.

Tracking multiple moving targets allows quantitative measure of the dynamic behavior in systems as diverse as animal groups in biology, turbulence in fluid dynamics and crowd and traffic control. In three dimensions, tracking several targets becomes increasingly hard since optical occlusions are very likely, i.e., two featureless targets frequently overlap for several frames. Occlusions are particularly frequent in biological groups such as bird flocks, fish schools, and insect swarms, a fact that has severely limited collective animal behavior field studies in the past. This paper presents a 3D tracking method that is robust in the case of severe occlusions. To ensure robustness, we adopt a global optimization approach that works on all objects and frames at once. To achieve practicality and scalability, we employ a divide and conquer formulation, thanks to which the computational complexity of the problem is reduced by orders of magnitude. We tested our algorithm with synthetic data, with experimental data of bird flocks and insect swarms and with public benchmark datasets, and show that our system yields high quality trajectories for hundreds of moving targets with severe overlap. The results obtained on very heterogeneous data show the potential applicability of our method to the most diverse experimental situations.

Short-range interactions versus long-range correlations in bird flocks.

Bird flocks are a paradigmatic example of collective motion. One of the prominent traits of flocking is the presence of long range velocity correlations between individuals, which allow them to influence each other over the large scales, keeping a high level of group coordination. A crucial question is to understand what is the mutual interaction between birds generating such nontrivial correlations. Here we use the maximum entropy (ME) approach to infer from experimental data of natural flocks the effective interactions between individuals. Compared to previous studies, we make a significant step forward as we retrieve the full functional dependence of the interaction on distance, and find that it decays exponentially over a range of a few individuals. The fact that ME gives a short-range interaction even though its experimental input is the long-range correlation function, shows that the method is able to discriminate the relevant information encoded in such correlations and single out a minimal number of effective parameters. Finally, we show how the method can be used to capture the degree of anisotropy of mutual interactions.

Emergence of collective changes in travel direction of starling flocks from individual birds' fluctuations.

One of the most impressive features of moving animal groups is their ability to perform sudden coherent changes in travel direction. While this collective decision can be a response to an external alarm cue, directional switching can also emerge from the intrinsic fluctuations in individual behaviour. However, the cause and the mechanism by which such collective changes of direction occur are not fully understood yet. Here, we present an experimental study of spontaneous collective turns in natural flocks of starlings. We employ a recently developed tracking algorithm to reconstruct three-dimensional trajectories of each individual bird in the flock for the whole duration of a turning event. Our approach enables us to analyse changes in the individual behaviour of every group member and reveal the emergent dynamics of turning. We show that spontaneous turns start from individuals located at the elongated tips of the flocks, and then propagate through the group. We find that birds on the tips deviate from the mean direction of motion much more frequently than other individuals, indicating that persistent localized fluctuations are the crucial ingredient for triggering a collective directional change. Finally, we quantitatively verify that birds follow equal-radius paths during turning, the effects of which are a change of the flock's orientation and a redistribution of individual locations in the group.

Specific Heat Anomaly in a Supercooled Liquid with Amorphous Boundary Conditions.

We study the specific heat of a model supercooled liquid confined in a spherical cavity with amorphous boundary conditions. We find the equilibrium specific heat has a cavity-size-dependent peak as a function of temperature. The cavity allows us to perform a finite-size scaling (FSS) analysis, which indicates that the peak persists at a finite temperature in the thermodynamic limit. We attempt to collapse the data onto a FSS curve according to different theoretical scenarios, obtaining reasonable results in two cases: a "not-so-simple" liquid with nonstandard values of the exponents α and ν, and random first-order theory, with two different length scales.

Silent flocks: constraints on signal propagation across biological groups.

Experiments find coherent information transfer through biological groups on length and time scales distinctly below those on which asymptotically correct hydrodynamic theories apply. We present here a new continuum theory of collective motion coupling the velocity and density fields of Toner and Tu to the inertial spin field recently introduced to describe information propagation in natural flocks of birds. The long-wavelength limit of the new equations reproduces the Toner-Tu theory, while at shorter wavelengths (or, equivalently, smaller damping), spin fluctuations dominate over density fluctuations, and second-sound propagation of the kind observed in real flocks emerges. We study the dispersion relation of the new theory and find that when the speed of second sound is large, a gap in momentum space sharply separates first- from second-sound modes. This gap implies the existence of silent flocks, namely, of medium-sized systems across which information cannot propagate in a linear and underdamped way, either under the form of orientational fluctuations or under that of density fluctuations, making it hard for the group to achieve coordination.

Finite-size scaling as a way to probe near-criticality in natural swarms.

Collective behavior in biological systems is often accompanied by strong correlations. The question has therefore arisen of whether correlation is amplified by the vicinity to some critical point in the parameters space. Biological systems, though, are typically quite far from the thermodynamic limit, so that the value of the control parameter at which correlation and susceptibility peak depend on size. Hence, a system would need to readjust its control parameter according to its size in order to be maximally correlated. This readjustment, though, has never been observed experimentally. By gathering three-dimensional data on swarms of midges in the field we find that swarms tune their control parameter and size so as to maintain a scaling behavior of the correlation function. As a consequence, correlation length and susceptibility scale with the system's size and swarms exhibit a near-maximal degree of correlation at all sizes.

Information transfer and behavioural inertia in starling flocks.

Collective decision-making in biological systems requires all individuals in the group to go through a behavioural change of state. During this transition fast and robust transfer of information is essential to prevent cohesion loss. The mechanism by which natural groups achieve such robustness, though, is not clear. Here we present an experimental study of starling flocks performing collective turns. We find that information about direction changes propagates across the flock with a linear dispersion law and negligible attenuation, hence minimizing group decoherence. These results contrast starkly with current models of collective motion, which predict diffusive transport of information. Building on spontaneous symmetry breaking and conservation laws arguments, we formulate a new theory that correctly reproduces linear and undamped propagation. Essential to the new framework is the inclusion of the birds' behavioural inertia. The new theory not only explains the data, but also predicts that information transfer must be faster the stronger the group's orientational order, a prediction accurately verified by the data. Our results suggest that swift decision-making may be the adaptive drive for the strong behavioural polarization observed in many living groups.

Collective behaviour without collective order in wild swarms of midges.

Collective behaviour is a widespread phenomenon in biology, cutting through a huge span of scales, from cell colonies up to bird flocks and fish schools. The most prominent trait of collective behaviour is the emergence of global order: individuals synchronize their states, giving the stunning impression that the group behaves as one. In many biological systems, though, it is unclear whether global order is present. A paradigmatic case is that of insect swarms, whose erratic movements seem to suggest that group formation is a mere epiphenomenon of the independent interaction of each individual with an external landmark. In these cases, whether or not the group behaves truly collectively is debated. Here, we experimentally study swarms of midges in the field and measure how much the change of direction of one midge affects that of other individuals. We discover that, despite the lack of collective order, swarms display very strong correlations, totally incompatible with models of non-interacting particles. We find that correlation increases sharply with the swarm's density, indicating that the interaction between midges is based on a metric perception mechanism. By means of numerical simulations we demonstrate that such growing correlation is typical of a system close to an ordering transition. Our findings suggest that correlation, rather than order, is the true hallmark of collective behaviour in biological systems.