Mosquito sound communication: are male swarms loud enough to attract females?

Given the unsurpassed sound sensitivity of mosquitoes among arthropods and the sound source power required for long-range hearing, we investigated the distance over which female mosquitoes detect species-specific cues in the sound of station-keeping mating swarms. A common misunderstanding, that mosquitoes cannot hear at long range because their hearing organs are ‘particle-velocity’ receptors, has clouded the fact that particle velocity is an intrinsic component of sound whatever the distance to the sound source. We exposed free-flying Anopheles coluzzii females to pre-recorded sounds of male An. coluzzii and An. gambiae s.s. swarms over a range of natural sound levels. Sound levels tested were related to equivalent distances between the female and the swarm for a given number of males, enabling us to infer distances over which females might hear large male swarms. We show that females do not respond to swarm sound up to 48 dB sound pressure level (SPL) and that louder SPLs are not ecologically relevant for a swarm. Considering that swarms are the only mosquito sound source that would be loud enough to be heard at long range, we conclude that inter-mosquito acoustic communication is restricted to close-range pair interactions. We also showed that the sensitivity to sound in free-flying males is much enhanced compared to that of tethered ones.     

Determining asymptotically large population sizes in insect swarms

Social animals commonly form aggregates that exhibit emergent collective behaviour, with group dynamics that are distinct from the behaviour of individuals. Simple models can qualitatively reproduce such behaviour, but only with large numbers of individuals. But how rapidly do the collective properties of animal aggregations in nature emerge with group size? Here, we study swarms of Chironomus riparius midges and measure how their statistical properties change as a function of the number of participating individuals. Once the swarms contain order 10 individuals, we find that all statistics saturate and the swarms enter an asymptotic regime. The influence of environmental cues on the swarm morphology decays on a similar scale. Our results provide a strong constraint on how rapidly swarm models must produce collective states. But our findings support the feasibility of using swarms as a design template for multi-agent systems, because self-organized states are possible even with few agents.     

Reconstructing the flight kinematics of swarming and mating in wild mosquitoes

We describe a novel tracking system for reconstructing three-dimensional tracks of individual mosquitoes in wild swarms and present the results of validating the system by filming swarms and mating events of the malaria mosquito Anopheles gambiae in Mali. The tracking system is designed to address noisy, low frame-rate (25 frames per second) video streams from a stereo camera system. Because flying A. gambiae move at 1–4 m s⁻¹, they appear as faded streaks in the images or sometimes do not appear at all. We provide an adaptive algorithm to search for missing streaks and a likelihood function that uses streak endpoints to extract velocity information. A modified multi-hypothesis tracker probabilistically addresses occlusions and a particle filter estimates the trajectories. The output of the tracking algorithm is a set of track segments with an average length of 0.6–1 s. The segments are verified and combined under human supervision to create individual tracks up to the duration of the video (90 s). We evaluate tracking performance using an established metric for multi-target tracking and validate the accuracy using independent stereo measurements of a single swarm. Three-dimensional reconstructions of A. gambiae swarming and mating events are presented.     

Do small swarms have an advantage when house hunting? The effect of swarm size on nest-site selection by Apis mellifera

Reproductive swarms of honeybees are faced with the problem of finding a good site to establish a new colony. We examined the potential effects of swarm size on the quality of nest-site choice through a combination of modelling and field experiments. We used an individual-based model to examine the effects of swarm size on decision accuracy under the assumption that the number of bees actively involved in the decision-making process (scouts) is an increasing function of swarm size. We found that the ability of a swarm to choose the best of two nest sites decreases as swarm size increases when there is some time-lag between discovering the sites, consistent with Janson & Beekman (Janson & Beekman 2007 Proceedings of European Conference on Complex Systems, pp. 204–211.). However, when simulated swarms were faced with a realistic problem of choosing between many nest sites discoverable at all times, larger swarms were more accurate in their decisions than smaller swarms owing to their ability to discover nest sites more rapidly. Our experimental fieldwork showed that large swarms invest a larger number of scouts into the decision-making process than smaller swarms. Preliminary analysis of waggle dances from experimental swarms also suggested that large swarms could indeed discover and advertise nest sites at a faster rate than small swarms.     

Understanding how bacterial collectives organize on surfaces by tracking surfactant flow

Swarming is a collective bacterial behavior in which a dense population of bacterial cells moves over a porous surface, resulting in the expansion of the population. This collective behavior can guide bacteria away from potential stressors such as antibiotics and bacterial viruses. However, the mechanisms responsible for the organization of swarms are not understood. Here, we briefly review models that are based on bacterial sensing and fluid mechanics that are proposed to guide swarming in the pathogenic bacterium Pseudomonas aeruginosa. To provide further insight into the role of fluid mechanics in P. aeruginosa swarms, we track the movement of tendrils and the flow of surfactant using a novel technique that we have developed, Imaging of Reflected Illuminated Structures (IRIS). Our measurements show that tendrils and surfactants form distinct layers that grow in lockstep with each other. The results raise new questions about existing swarming models and the possibility that the flow of surfactants impacts tendril development. These findings emphasize that swarm organization involves an interplay between biological processes and fluid mechanics.     

Metachronal waves in the flagellar beating of Volvox and their hydrodynamic origin

Groups of eukaryotic cilia and flagella are capable of coordinating their beating over large scales, routinely exhibiting collective dynamics in the form of metachronal waves. The origin of this behaviour—possibly influenced by both mechanical interactions and direct biological regulation—is poorly understood, in large part due to a lack of quantitative experimental studies. Here we characterize in detail flagellar coordination on the surface of the multicellular alga Volvox carteri, an emerging model organism for flagellar dynamics. Our studies reveal for the first time that the average metachronal coordination observed is punctuated by periodic phase defects during which synchrony is partial and limited to specific groups of cells. A minimal model of hydrodynamically coupled oscillators can reproduce semi-quantitatively the characteristics of the average metachronal dynamics, and the emergence of defects. We systematically study the model''s behaviour by assessing the effect of changing intrinsic rotor characteristics, including oscillator stiffness and the nature of their internal driving force, as well as their geometric properties and spatial arrangement. Our results suggest that metachronal coordination follows from deformations in the oscillators'' limit cycles induced by hydrodynamic stresses, and that defects result from sufficiently steep local biases in the oscillators'' intrinsic frequencies. Additionally, we find that random variations in the intrinsic rotor frequencies increase the robustness of the average properties of the emergent metachronal waves.     

A dynamic broadband reflector built from microscopic silica spheres in the ‘disco’ clam Ctenoides ales

The ‘disco’ or ‘electric’ clam Ctenoides ales (Limidae) is the only species of bivalve known to have a behaviourally mediated photic display. This display is so vivid that it has been repeatedly confused for bioluminescence, but it is actually the result of scattered light. The flashing occurs on the mantle lip, where electron microscopy revealed two distinct tissue sides: one highly scattering side that contains dense aggregations of spheres composed of silica, and one highly absorbing side that does not. High-speed video confirmed that the two sides act in concert to alternate between vivid broadband reflectance and strong absorption in the blue region of the spectrum. Optical modelling suggests that the diameter of the spheres is nearly optimal for scattering visible light, especially at shorter wavelengths which predominate in their environment. This simple mechanism produces a striking optical effect that may function as a signal.     

A framework for understanding the architecture of collective movements using pairwise analyses of animal movement data

The study of collective or group-level movement patterns can provide insight regarding the socio-ecological interface, the evolution of self-organization and mechanisms of inter-individual information exchange. The suite of drivers influencing coordinated movement trajectories occur across scales, resulting from regular annual, seasonal and circadian stimuli and irregular intra- or interspecific interactions and environmental encounters acting on individuals. Here, we promote a conceptual framework with an associated statistical machinery to quantify the type and degree of synchrony, spanning absence to complete, in pairwise movements. The application of this framework offers a foundation for detailed understanding of collective movement patterns and causes. We emphasize the use of Fourier and wavelet approaches of measuring pairwise movement properties and illustrate them with simulations that contain different types of complexity in individual movement, correlation in movement stochasticity, and transience in movement relatedness. Application of this framework to movements of free-ranging African elephants (Loxodonta africana) provides unique insight on the separate roles of sociality and ecology in the fission–fusion society of these animals, quantitatively characterizing the types of bonding that occur at different levels of social relatedness in a movement context. We conclude with a discussion about expanding this framework to the context of larger (greater than three) groups towards understanding broader population and interspecific collective movement patterns and their mechanisms.     

Emergent behavioural phenotypes of swarming models revealed by mimicking a frustrated anti-ferromagnet

Self-propelled particle (SPP) models are often compared with animal swarms. However, the collective animal behaviour observed in experiments often leaves considerable unconstrained freedom in the structure of a proposed model. Essentially, multiple models can describe the observed behaviour of animal swarms in simple environments. To tackle this degeneracy, we study swarms of SPPs in non-trivial environments as a new approach to distinguish between candidate models. We restrict swarms of SPPs to circular (periodic) channels where they polarize in one of two directions (like spins) and permit information to pass through windows between neighbouring channels. Co-alignment between particles then couples the channels (anti-ferromagnetically) so that they tend to counter-rotate. We study channels arranged to mimic a geometrically frustrated anti-ferromagnet and show how the effects of this frustration allow us to better distinguish between SPP models. Similar experiments could therefore improve our understanding of collective motion in animals. Finally, we discuss how the spin analogy can be exploited to construct universal logic gates, and therefore swarming systems that can function as Turing machines.     

Mechanics regulates ATP-stimulated collective calcium response in fibroblast cells

Cells constantly sense their chemical and mechanical environments. We study the effect of mechanics on the ATP-induced collective calcium response of fibroblast cells in experiments that mimic various tissue environments. We find that closely packed two-dimensional cell cultures on a soft polyacrylamide gel (Young''s modulus E = 690 Pa) contain more cells exhibiting calcium oscillations than cultures on a rigid substrate (E = 36 000 Pa). Calcium responses of cells on soft substrates show a slower decay of calcium level relative to those on rigid substrates. Actin enhancement and disruption experiments for the cell cultures allow us to conclude that actin filaments determine the collective Ca²⁺ oscillatory behaviour in the culture. Inhibition of gap junctions results in a decrease of the oscillation period and reduced correlation of calcium responses, which suggests additional complexity of signalling upon cell–cell contact. Moreover, the frequency of calcium oscillations is independent of the rigidity of the substrate but depends on ATP concentration. We compare our results with those from similar experiments on individual cells. Overall, our observations show that collective chemical signalling in cell cultures via calcium depends critically on the mechanical environment.     

The entropic basis of collective behaviour

We identify a unique viewpoint on the collective behaviour of intelligent agents. We first develop a highly general abstract model for the possible future lives these agents may encounter as a result of their decisions. In the context of these possibilities, we show that the causal entropic principle, whereby agents follow behavioural rules that maximize their entropy over all paths through the future, predicts many of the observed features of social interactions among both human and animal groups. Our results indicate that agents are often able to maximize their future path entropy by remaining cohesive as a group and that this cohesion leads to collectively intelligent outcomes that depend strongly on the distribution of the number of possible future paths. We derive social interaction rules that are consistent with maximum entropy group behaviour for both discrete and continuous decision spaces. Our analysis further predicts that social interactions are likely to be fundamentally based on Weber''s law of response to proportional stimuli, supporting many studies that find a neurological basis for this stimulus–response mechanism and providing a novel basis for the common assumption of linearly additive ‘social forces’ in simulation studies of collective behaviour.     

Predator confusion is sufficient to evolve swarming behaviour

Swarming behaviours in animals have been extensively studied owing to their implications for the evolution of cooperation, social cognition and predator–prey dynamics. An important goal of these studies is discerning which evolutionary pressures favour the formation of swarms. One hypothesis is that swarms arise because the presence of multiple moving prey in swarms causes confusion for attacking predators, but it remains unclear how important this selective force is. Using an evolutionary model of a predator–prey system, we show that predator confusion provides a sufficient selection pressure to evolve swarming behaviour in prey. Furthermore, we demonstrate that the evolutionary effect of predator confusion on prey could in turn exert pressure on the structure of the predator''s visual field, favouring the frontally oriented, high-resolution visual systems commonly observed in predators that feed on swarming animals. Finally, we provide evidence that when prey evolve swarming in response to predator confusion, there is a change in the shape of the functional response curve describing the predator''s consumption rate as prey density increases. Thus, we show that a relatively simple perceptual constraint—predator confusion—could have pervasive evolutionary effects on prey behaviour, predator sensory mechanisms and the ecological interactions between predators and prey.     

Fast,high-throughput measurement of collective behaviour in a bacterial population

Swimming bacteria explore their environment by performing a random walk, which is biased in response to, for example, chemical stimuli, resulting in a collective drift of bacterial populations towards ‘a better life’. This phenomenon, called chemotaxis, is one of the best known forms of collective behaviour in bacteria, crucial for bacterial survival and virulence. Both single-cell and macroscopic assays have investigated bacterial behaviours. However, theories that relate the two scales have previously been difficult to test directly. We present an image analysis method, inspired by light scattering, which measures the average collective motion of thousands of bacteria simultaneously. Using this method, a time-varying collective drift as small as 50 nm s⁻¹ can be measured. The method, validated using simulations, was applied to chemotactic Escherichia coli bacteria in linear gradients of the attractant α-methylaspartate. This enabled us to test a coarse-grained minimal model of chemotaxis. Our results clearly map the onset of receptor methylation, and the transition from linear to logarithmic sensing in the bacterial response to an external chemoeffector. Our method is broadly applicable to problems involving the measurement of collective drift with high time resolution, such as cell migration and fluid flows measurements, and enables fast screening of tactic behaviours.     

Isotropic microscale mechanical properties of coral skeletons

Scleractinian corals are a major source of biogenic calcium carbonate, yet the relationship between their skeletal microstructure and mechanical properties has been scarcely studied. In this work, the skeletons of two coral species: solitary Balanophyllia europaea and colonial Stylophora pistillata, were investigated by nanoindentation. The hardness H_IT and Young''s modulus E_IT were determined from the analysis of several load–depth data on two perpendicular sections of the skeletons: longitudinal (parallel to the main growth axis) and transverse. Within the experimental and statistical uncertainty, the average values of the mechanical parameters are independent on the section''s orientation. The hydration state of the skeletons did not affect the mechanical properties. The measured values, E_IT in the 76–77 GPa range, and H_IT in the 4.9–5.1 GPa range, are close to the ones expected for polycrystalline pure aragonite. Notably, a small difference in H_IT is observed between the species. Different from corals, single-crystal aragonite and the nacreous layer of the seashell Atrina rigida exhibit clearly orientation-dependent mechanical properties. The homogeneous and isotropic mechanical behaviour of the coral skeletons at the microscale is correlated with the microstructure, observed by electron microscopy and atomic force microscopy, and with the X-ray diffraction patterns of the longitudinal and transverse sections.     

Fish and robots swimming together: attraction towards the robot demands biomimetic locomotion

The integration of biomimetic robots in a fish school may enable a better understanding of collective behaviour, offering a new experimental method to test group feedback in response to behavioural modulations of its ‘engineered’ member. Here, we analyse a robotic fish and individual golden shiners (Notemigonus crysoleucas) swimming together in a water tunnel at different flow velocities. We determine the positional preference of fish with respect to the robot, and we study the flow structure using a digital particle image velocimetry system. We find that biomimetic locomotion is a determinant of fish preference as fish are more attracted towards the robot when its tail is beating rather than when it is statically immersed in the water as a ‘dummy’. At specific conditions, the fish hold station behind the robot, which may be due to the hydrodynamic advantage obtained by swimming in the robot''s wake. This work makes a compelling case for the need of biomimetic locomotion in promoting robot–animal interactions and it strengthens the hypothesis that biomimetic robots can be used to study and modulate collective animal behaviour.     

Whirligig beetles as corralled active Brownian particles

We study the collective dynamics of groups of whirligig beetles Dineutus discolor (Coleoptera: Gyrinidae) swimming freely on the surface of water. We extract individual trajectories for each beetle, including positions and orientations, and use this to discover (i) a density-dependent speed scaling like v ∼ ρ^−ν with ν ≈ 0.4 over two orders of magnitude in density (ii) an inertial delay for velocity alignment of approximately 13 ms and (iii) coexisting high and low-density phases, consistent with motility-induced phase separation (MIPS). We modify a standard active Brownian particle (ABP) model to a corralled ABP (CABP) model that functions in open space by incorporating a density-dependent reorientation of the beetles, towards the cluster. We use our new model to test our hypothesis that an motility-induced phase separation (MIPS) (or a MIPS like effect) can explain the co-occurrence of high- and low-density phases we see in our data. The fitted model then successfully recovers a MIPS-like condensed phase for N = 200 and the absence of such a phase for smaller group sizes N = 50, 100.     

Contact inhibition of locomotion probabilities drive solitary versus collective cell migration

Contact inhibition of locomotion (CIL) is the process whereby cells collide, cease migrating in the direction of the collision, and repolarize their migration machinery away from the collision. Quantitative analysis of CIL has remained elusive because cell-to-cell collisions are infrequent in traditional cell culture. Moreover, whereas CIL predicts mutual cell repulsion and ‘scattering’ of cells, the same cells in vivo are observed to undergo CIL at some developmental times and collective cell migration at others. It remains unclear whether CIL is simply absent during collective cell migration, or if the two processes coexist and are perhaps even related. Here, we used micropatterned stripes of extracellular matrix to restrict cell migration to linear paths such that cells polarized in one of two directions and collisions between cells occurred frequently and consistently, permitting quantitative and unbiased analysis of CIL. Observing repolarization events in different contexts, including head-to-head collision, head-to-tail collision, collision with an inert barrier, or no collision, and describing polarization as a two-state transition indicated that CIL occurs probabilistically, and most strongly upon head-to-head collisions. In addition to strong CIL, we also observed ‘trains’ of cells moving collectively with high persistence that appeared to emerge from single cells. To reconcile these seemingly conflicting observations of CIL and collective cell migration, we constructed an agent-based model to simulate our experiments. Our model quantitatively predicted the emergence of collective migration, and demonstrated the sensitivity of such emergence to the probability of CIL. Thus CIL and collective migration can coexist, and in fact a shift in CIL probabilities may underlie transitions between solitary cell migration and collective cell migration. Taken together, our data demonstrate the emergence of persistently polarized, collective cell movement arising from CIL between colliding cells.     

Collective cell migration: leadership,invasion and segregation

A number of biological processes, such as embryo development, cancer metastasis or wound healing, rely on cells moving in concert. The mechanisms leading to the emergence of coordinated motion remain however largely unexplored. Although biomolecular signalling is known to be involved in most occurrences of collective migration, the role of physical and mechanical interactions has only been recently investigated. In this study, a versatile framework for cell motility is implemented in silico in order to study the minimal requirements for the coordination of a group of epithelial cells. We find that cell motility and cell–cell mechanical interactions are sufficient to generate a broad array of behaviours commonly observed in vitro and in vivo. Cell streaming, sheet migration and susceptibility to leader cells are examples of behaviours spontaneously emerging from these simple assumptions, which might explain why collective effects are so ubiquitous in nature. The size of the population and its confinement appear, in particular, to play an important role in the coordination process. In all cases, the complex response of the population can be predicted from the knowledge of the correlation length of the velocity field measured in the bulk of the epithelial layer. This analysis provides also new insights into cancer metastasis and cell sorting, suggesting, in particular, that collective invasion might result from an emerging coordination in a system where single cells are mechanically unable to invade.     

Periodic dynamics of coupled cell networks II: cyclic symmetry

A coupled cell network is a directed graph whose nodes represent dynamical systems and whose directed edges specify how those systems are coupled to each other. The typical dynamic behaviour of a network is strongly constrained by its topology. Especially important constraints arise from global (group) symmetries and local (groupoid) symmetries. The H/K theorem of Buono and Golubitsky characterises the possible spatio-temporal symmetries of time-periodic states of group-equivariant dynamical systems. A version of this theorem for group-symmetric networks has been proved by Josi? and Török. In networks, spatial symmetries correspond to synchrony of cells, and spatio-temporal symmetries correspond to phase relations between cells. Associated with any coupled cell network is a canonical class of admissible ODEs that respect the network topology. A pattern of synchrony or phase relations in a hyperbolic time-periodic state of such an ODE is rigid if the pattern persists under small admissible perturbations. We characterise rigid patterns of synchrony and rigid phase patterns in coupled cell networks, on the assumption that the periodic state is fully oscillatory (no cell is in equilibrium) and the network has a basic property, the rigid phase property. We conjecture that all networks have the rigid phase property, and that in any path-connected network an admissible ODE with a hyperbolic periodic state can always be perturbed to make the perturbed periodic state fully oscillatory. Our main result states that in any path-connected network with the rigid phase property, every rigid pattern of phase relations can be characterised in two stages. First, sets of cells form synchronous clumps according to a balanced equivalence relation. Second, the corresponding quotient network has a cyclic group of automorphisms, and the phase relations are induced by associating a fixed phase shift with a generator of this group. Thus the clumps of synchronous cells form a discrete rotating wave. As a corollary, we prove an analogue of the H/K theorem for any path-connected network. We also discuss the non-path-connected case.     

Lifetime Measurements in 178Hf

Lifetimes of levels from K^π = 2⁺, K^π = 4⁺ and several K^π = 0⁺ bands have been measured in the ¹⁷⁸Hf nucleus using the GRID technique. Lifetimes of the 2⁺ and 3⁺ levels were measured within the K^π = 2⁺ γ band. A lower limit was established for the lifetime of the 4⁺ level of the K^π = 4⁺ band. The resulting upper limits for the absolute B(E2) values exclude collective transitions from the K^π = 4⁺ to the ground state band but not to the K^π= 2⁺ band. Level lifetimes were also measured for several states within three separate K^π= 0⁺ bands. Evidence is presented for a previously unobserved case of two excited K^π= 0⁺ bands being connected via collective E2 transitions.