Personality composition is more important than group size in determining collective foraging behaviour in the wild

Describing the factors that shape collective behaviour is central to our understanding of animal societies. Countless studies have demonstrated an effect of group size in the emergence of collective behaviours, but comparatively few have accounted for the composition/diversity of behavioural phenotypes, which is often conflated with group size. Here, we simultaneously examine the effect of personality composition and group size on nest architecture and collective foraging aggressiveness in the social spider Stegodyphus dumicola. We created colonies of two different sizes (10 or 30 individuals) and four compositions of boldness (all bold, all shy, mixed bold and shy, or average individuals) in the field and then measured their collective behaviour. Larger colonies produced bigger capture webs, while colonies containing a higher proportion of bold individuals responded to and attacked prey more rapidly. The number of attackers during collective foraging was determined jointly by composition and size, although composition had an effect size more than twice that of colony size: our results suggest that colonies of just 10 bold spiders would attack prey with as many attackers as colonies of 110 ‘average’ spiders. Thus, personality composition is a more potent (albeit more cryptic) determinant of collective foraging in these societies.     

Diffusion of individual birds in starling flocks

Flocking is a paradigmatic example of collective animal behaviour, where global order emerges out of self-organization. Each individual has a tendency to align its flight direction with those of neighbours, and such a simple form of interaction produces a state of collective motion of the group. When compared with other cases of collective ordering, a crucial feature of animal groups is that the interaction network is not fixed in time, as each individual moves and continuously changes its neighbours. The possibility to exchange neighbours strongly enhances the stability of global ordering and the way information is propagated through the group. Here, we assess the relevance of this mechanism in large flocks of starlings (Sturnus vulgaris). We find that birds move faster than Brownian walkers both with respect to the centre of mass of the flock, and with respect to each other. Moreover, this behaviour is strongly anisotropic with respect to the direction of motion of the flock. We also measure the amount of neighbours reshuffling and find that neighbours change in time exclusively as a consequence of the random fluctuations in the individual motion, so that no specific mechanism to keep one''s neighbours seems to be enforced. On the contrary, our findings suggest that a more complex dynamical process occurs at the border of the flock.     

The dynamics of sperm cooperation in a competitive environment

Sperm cooperation has evolved in a variety of taxa and is often considered a response to sperm competition, yet the benefit of this form of collective movement remains unclear. Here, we use fine-scale imaging and a minimal mathematical model to study sperm aggregation in the rodent genus Peromyscus. We demonstrate that as the number of sperm cells in an aggregate increase, the group moves with more persistent linearity but without increasing speed. This benefit, however, is offset in larger aggregates as the geometry of the group forces sperm to swim against one another. The result is a non-monotonic relationship between aggregate size and average velocity with both a theoretically predicted and empirically observed optimum of six to seven sperm per aggregate. To understand the role of sexual selection in driving these sperm group dynamics, we compared two sister-species with divergent mating systems. We find that sperm of Peromyscus maniculatus (highly promiscuous), which have evolved under intense competition, form optimal-sized aggregates more often than sperm of Peromyscus polionotus (strictly monogamous), which lack competition. Our combined mathematical and experimental study of coordinated sperm movement reveals the importance of geometry, motion and group size on sperm velocity and suggests how these physical variables interact with evolutionary selective pressures to regulate cooperation in competitive environments.     

The limits of convergence in the collective behavior of competing marine taxa

Collective behaviors in biological systems such as coordinated movements have important ecological and evolutionary consequences. While many studies examine within‐species variation in collective behavior, explicit comparisons between functionally similar species from different taxonomic groups are rare. Therefore, a fundamental question remains: how do collective behaviors compare between taxa with morphological and physiological convergence, and how might this relate to functional ecology and niche partitioning? We examined the collective motion of two ecologically similar species from unrelated clades that have competed for pelagic predatory niches for over 500 million years—California market squid, Doryteuthis opalescens (Mollusca) and Pacific sardine, Sardinops sagax (Chordata). We (1) found similarities in how groups of individuals from each species collectively aligned, measured by angular deviation, the difference between individual orientation and average group heading. We also (2) show that conspecific attraction, which we approximated using nearest neighbor distance, was greater in sardine than squid. Finally, we (3) found that individuals of each species explicitly matched the orientation of groupmates, but that these matching responses were less rapid in squid than sardine. Based on these results, we hypothesize that information sharing is a comparably important function of social grouping for both taxa. On the other hand, some capabilities, including hydrodynamically conferred energy savings and defense against predators, could stem from taxon‐specific biology.     

Individual-level personality influences social foraging and collective behaviour in wild birds

There is increasing evidence that animal groups can maintain coordinated behaviour and make collective decisions based on simple interaction rules. Effective collective action may be further facilitated by individual variation within groups, particularly through leader–follower polymorphisms. Recent studies have suggested that individual-level personality traits influence the degree to which individuals use social information, are attracted to conspecifics, or act as leaders/followers. However, evidence is equivocal and largely limited to laboratory studies. We use an automated data-collection system to conduct an experiment testing the relationship between personality and collective decision-making in the wild. First, we report that foraging flocks of great tits (Parus major) show strikingly synchronous behaviour. A predictive model of collective decision-making replicates patterns well, suggesting simple interaction rules are sufficient to explain the observed social behaviour. Second, within groups, individuals with more reactive personalities behave more collectively, moving to within-flock areas of higher density. By contrast, proactive individuals tend to move to and feed at spatial periphery of flocks. Finally, comparing alternative simulations of flocking with empirical data, we demonstrate that variation in personality promotes within-patch movement while maintaining group cohesion. Our results illustrate the importance of incorporating individual variability in models of social behaviour.     

Diffusion and Topological Neighbours in Flocks of Starlings: Relating a Model to Empirical Data

Moving in a group while avoiding collisions with group members causes internal dynamics in the group. Although these dynamics have recently been measured quantitatively in starling flocks (Sturnus vulgaris), it is unknown what causes them. Computational models have shown that collective motion in groups is likely due to attraction, avoidance and, possibly, alignment among group members. Empirical studies show that starlings adjust their movement to a fixed number of closest neighbours or topological range, namely 6 or 7 and assume that each of the three activities is done with the same number of neighbours (topological range). Here, we start from the hypothesis that escape behavior is more effective at preventing collisions in a flock when avoiding the single closest neighbor than compromising by avoiding 6 or 7 of them. For alignment and attraction, we keep to the empirical topological range. We investigate how avoiding one or several neighbours affects the internal dynamics of flocks of starlings in our computational model StarDisplay. By comparing to empirical data, we confirm that internal dynamics resemble empirical data more closely if flock members avoid merely their single, closest neighbor. Our model shows that considering a different number of interaction partners per activity represents a useful perspective and that changing a single parameter, namely the number of interaction partners that are avoided, has several effects through selforganisation.     

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.     

Minimal Network Topologies for Signal Processing during Collective Cell Chemotaxis

Cell-cell communication plays an important role in collective cell migration. However, it remains unclear how cells in a group cooperatively process external signals to determine the group’s direction of motion. Although the topology of signaling pathways is vitally important in single-cell chemotaxis, the signaling topology for collective chemotaxis has not been systematically studied. Here, we combine mathematical analysis and simulations to find minimal network topologies for multicellular signal processing in collective chemotaxis. We focus on border cell cluster chemotaxis in the Drosophila egg chamber, in which responses to several experimental perturbations of the signaling network are known. Our minimal signaling network includes only four elements: a chemoattractant, the protein Rac (indicating cell activation), cell protrusion, and a hypothesized global factor responsible for cell-cell interaction. Experimental data on cell protrusion statistics allows us to systematically narrow the number of possible topologies from more than 40,000,000 to only six minimal topologies with six interactions between the four elements. This analysis does not require a specific functional form of the interactions, and only qualitative features are needed; it is thus robust to many modeling choices. Simulations of a stochastic biochemical model of border cell chemotaxis show that the qualitative selection procedure accurately determines which topologies are consistent with the experiment. We fit our model for all six proposed topologies; each produces results that are consistent with all experimentally available data. Finally, we suggest experiments to further discriminate possible pathway topologies.     

Nutritional state and collective motion: from individuals to mass migration

In order to move effectively in unpredictable or heterogeneous environments animals must make appropriate decisions in response to internal and external cues. Identifying the link between these components remains a challenge for movement ecology and is important in understanding the mechanisms driving both individual and collective motion. One accessible way of examining how internal state influences an individual''s motion is to consider the nutritional state of an animal. Our experimental results reveal that nutritional state exerts a relatively minor influence on the motion of isolated individuals, but large group-level differences emerge from diet affecting inter-individual interactions. This supports the idea that mass movement in locusts may be driven by cannibalism. To estimate how these findings are likely to impact collective migration of locust hopper bands, we create an experimentally parametrized model of locust interactions and motion. Our model supports our hypothesis that nutrient-dependent social interactions can lead to the collective motion seen in our experiments and predicts a transition in the mean speed and the degree of coordination of bands with increasing insect density. Furthermore, increasing the interaction strength (representing greater protein deprivation) dramatically reduces the critical density at which this transition occurs, demonstrating that individuals'' nutritional state could have a major impact on large-scale migration.     

The legacy effects of keystone individuals on collective behaviour scale to how long they remain within a group

The collective behaviour of social groups is often strongly influenced by one or few individuals, termed here ‘keystone individuals’. We examined whether the influence of keystone individuals on collective behaviour lingers after their departure and whether these lingering effects scale with their tenure in the group. In the social spider, Stegodyphus dumicola, colonies'' boldest individuals wield a disproportionately large influence over colony behaviour. We experimentally manipulated keystones'' tenure in laboratory-housed colonies and tracked their legacy effects on collective prey capture following their removal. We found that bolder keystones caused more aggressive collective foraging behaviour and catalysed greater inter-individual variation in boldness within their colonies. The longer keystones remained in a colony, the longer both of these effects lingered after their departure. Our data demonstrate that, long after their disappearance, keystones have large and lasting effects on social dynamics at both the individual and colony levels.     

Disturbance and predation risk influence vigilance synchrony of black‐necked cranes Grus nigricollis,but not as strongly as expected

Animals monitor surrounding dangers independently or cooperatively (synchronized and coordinated vigilance), with independent and synchronized scanning being prevalent. Coordinated vigilance, including unique sentinel behavior, is rare in nature, since it is time‐consuming and limited in terms of benefits. No evidence showed animals adopt alternative vigilance strategies during antipredation scanning yet. Considering the nonindependent nature of both synchronization and coordination, we assessed whether group members could keep alert synchronously or in a coordinated fashion under different circumstance. We studied how human behavior and species‐specific variables impacted individual and collective vigilance of globally threatened black‐necked cranes (Grus nigricollis) and explored behavior‐based wildlife management. We tested both predation risk (number of juveniles in group) and human disturbance (level and distance) effects on individual and collective antipredation vigilance of black‐necked crane families. Adults spent significantly more time (proportion and duration) on scanning than juveniles, and parents with juveniles behaved more vigilant. Both adults and juveniles increased time allocation and duration on vigilance with observer proximity. Deviation between observed and expected collective vigilance varied with disturbance and predation risk from zero, but not significantly so, indicating that an independent vigilance strategy was adopted by black‐necked crane couples. The birds showed synchronized vigilance in low disturbance areas, with fewer juveniles and far from observers; otherwise, they scanned in coordinated fashion. The collective vigilance, from synchronized to coordinated pattern, varied as a function of observer distance that helped us determine a safe distance of 403.75 m for the most vulnerable family groups with two juveniles. We argue that vigilance could constitute a prime indicator in behavior‐based species conservation, and we suggesting a safe distance of at least 400 m should be considered in future tourist management.     

Innovation in the collective brain

Innovation is often assumed to be the work of a talented few, whose products are passed on to the masses. Here, we argue that innovations are instead an emergent property of our species'' cultural learning abilities, applied within our societies and social networks. Our societies and social networks act as collective brains. We outline how many human brains, which evolved primarily for the acquisition of culture, together beget a collective brain. Within these collective brains, the three main sources of innovation are serendipity, recombination and incremental improvement. We argue that rates of innovation are heavily influenced by (i) sociality, (ii) transmission fidelity, and (iii) cultural variance. We discuss some of the forces that affect these factors. These factors can also shape each other. For example, we provide preliminary evidence that transmission efficiency is affected by sociality—languages with more speakers are more efficient. We argue that collective brains can make each of their constituent cultural brains more innovative. This perspective sheds light on traits, such as IQ, that have been implicated in innovation. A collective brain perspective can help us understand otherwise puzzling findings in the IQ literature, including group differences, heritability differences and the dramatic increase in IQ test scores over time.     

From Schooling to Shoaling: Patterns of Collective Motion in Zebrafish (Danio rerio)

Animal groups on the move can take different configurations. For example, groups of fish can either be ‘shoals’ or ‘schools’: shoals are simply aggregations of individuals; schools are shoals exhibiting polarized, synchronized motion. Here we demonstrate that polarization distributions of groups of zebrafish (Danio rerio) are bimodal, showing two distinct modes of collective motion corresponding to the definitions of shoaling and schooling. Other features of the group''s motion also vary consistently between the two modes: zebrafish schools are faster and less dense than zebrafish shoals. Habituation to an environment can also alter the proportion of time zebrafish groups spend schooling or shoaling. Models of collective motion suggest that the degree and stability of group polarization increases with the group''s density. Examining zebrafish groups of different sizes from 5 to 50, we show that larger groups are less polarized than smaller groups. Decreased fearfulness in larger groups may function similarly to habituation, causing them to spend more time shoaling than schooling, contrary to most models'' predictions.     

Using multilayer network analysis to explore the temporal dynamics of collective behavior

Social organisms often show collective behaviors such as group foraging or movement.Collective behaviors can emerge from interactions between group members and may depend on the behavior of key individuals.When social interactions change over time,collective behaviors may change because these behaviors emerge from interactions among individuals.Despite the importance of,and growing interest in,the temporal dynamics of social interactions,it is not clear how to quantify changes in interactions over time or measure their stability.Furthermore,the temporal scale at which we should observe changes in social networks to detect biologically meaningful changes is not always apparent.Here we use multilayer network analysis to quantify temporal dynamics of social networks of the social spider Stegodyphus dumicola and determine how these dynamics relate to individual and group behaviors.We found that social interactions changed over time at a constant rate.Variation in both network structure and the identity of a keystone individual was not related to the mean or variance of the collective prey attack speed.Individuals that maintained a large and stable number of connections,despite changes in network structure,were the boldest individuals in the group.Therefore,social interactions and boldness are linked across time,but group collective behavior is not influenced by the stability of the social network.Our work demonstrates that dynamic social networks can be modeled in a multilayer framework.This approach may reveal biologically important temporal changes to social structure in other systems.     

Swarms of particle agents with harmonic interactions

Summary Agent-based modeling is a powerful methodology to describe the occurence of complex behavior in biological systems. The interaction of a large number of individuals (agents) may for example lead to the emergence of new forms of collective motion. In this paper, we investigate a particle-based approach to the coherent motion of a swarm with parabolic (i. e. harmonic) interactions between the agents. It is based on generalized Langevin equations for the particle agents, which take into account (i) energetic conditions for active motion, (ii) linear attractive forces between each two agents. The complex collective motion observed can be explained as the result of these different influences: the active motion of the agents, which is driven by the energy-take up, would eventually lead to a spatial dispersion of the swarm, while the mutual interaction of the agents results in a tendency of spatial concentration. In addition to particle-based computer simulations, we also provide a mathematical framework for investigating the collective dynamics. Dedicated to the memory of Michael Conrad     

CompuCell3D Simulations Reproduce Mesenchymal Cell Migration on Flat Substrates

Mesenchymal cell crawling is a critical process in normal development, in tissue function, and in many diseases. Quantitatively predictive numerical simulations of cell crawling thus have multiple scientific, medical, and technological applications. However, we still lack a low-computational-cost approach to simulate mesenchymal three-dimensional (3D) cell crawling. Here, we develop a computationally tractable 3D model (implemented as a simulation in the CompuCell3D simulation environment) of mesenchymal cells crawling on a two-dimensional substrate. The Fürth equation, the usual characterization of mean-squared displacement (MSD) curves for migrating cells, describes a motion in which, for increasing time intervals, cell movement transitions from a ballistic to a diffusive regime. Recent experiments have shown that for very short time intervals, cells exhibit an additional fast diffusive regime. Our simulations’ MSD curves reproduce the three experimentally observed temporal regimes, with fast diffusion for short time intervals, slow diffusion for long time intervals, and intermediate time -interval-ballistic motion. The resulting parameterization of the trajectories for both experiments and simulations allows the definition of time- and length scales that translate between computational and laboratory units. Rescaling by these scales allows direct quantitative comparisons among MSD curves and between velocity autocorrelation functions from experiments and simulations. Although our simulations replicate experimentally observed spontaneous symmetry breaking, short-timescale diffusive motion, and spontaneous cell-motion reorientation, their computational cost is low, allowing their use in multiscale virtual-tissue simulations. Comparisons between experimental and simulated cell motion support the hypothesis that short-time actomyosin dynamics affects longer-time cell motility. The success of the base cell-migration simulation model suggests its future application in more complex situations, including chemotaxis, migration through complex 3D matrices, and collective cell motion.     

Relating Lateralization of Eye Use to Body Motion in the Avoidance Behavior of the Chameleon (Chamaeleo chameleon)

Lateralization is mostly analyzed for single traits, but seldom for two or more traits while performing a given task (e.g. object manipulation). We examined lateralization in eye use and in body motion that co-occur during avoidance behaviour of the common chameleon, Chamaeleo chameleon. A chameleon facing a moving threat smoothly repositions its body on the side of its perch distal to the threat, to minimize its visual exposure. We previously demonstrated that during the response (i) eye use and body motion were, each, lateralized at the tested group level (N = 26), (ii) in body motion, we observed two similar-sized sub-groups, one exhibiting a greater reduction in body exposure to threat approaching from the left and one – to threat approaching from the right (left- and right-biased subgroups), (iii) the left-biased sub-group exhibited weak lateralization of body exposure under binocular threat viewing and none under monocular viewing while the right-biased sub-group exhibited strong lateralization under both monocular and binocular threat viewing. In avoidance, how is eye use related to body motion at the entire group and at the sub-group levels? We demonstrate that (i) in the left-biased sub-group, eye use is not lateralized, (ii) in the right-biased sub-group, eye use is lateralized under binocular, but not monocular viewing of the threat, (iii) the dominance of the right-biased sub-group determines the lateralization of the entire group tested. We conclude that in chameleons, patterns of lateralization of visual function and body motion are inter-related at a subtle level. Presently, the patterns cannot be compared with humans'' or related to the unique visual system of chameleons, with highly independent eye movements, complete optic nerve decussation and relatively few inter-hemispheric commissures. We present a model to explain the possible inter-hemispheric differences in dominance in chameleons'' visual control of body motion during avoidance.     

The effects of flow on schooling Devario aequipinnatus: school structure,startle response and information transmission

To assess how flow affects school structure and threat detection, startle response rates of solitary and small groups of giant danio Devario aequipinnatus to visual looming stimuli were compared in flow and no‐flow conditions. The instantaneous position and heading of each D. aequipinnatus was extracted from high‐speed videos. Behavioural results indicate that (1) school structure is altered in flow such that D. aequipinnatus orient upstream while spanning out in a crosswise direction, (2) the probability of at least one D. aequipinnatus detecting the visual looming stimulus is higher in flow than no flow for both solitary D. aequipinnatus and groups of eight D. aequipinnatus; however, (3) the probability of three or more individuals responding is higher in no flow than in flow. These results indicate a higher probability of stimulus detection in flow but a higher probability of internal transmission of information in no flow. Finally, results were well predicted by a computational model of collective fright response that included the probability of direct detection (based on signal detection theory) and indirect detection (i.e. via interactions between group members) of threatening stimuli. This model provides a new theoretical framework for analysing the collective transfer of information among groups of fishes and other organisms.     

From the first intention movement to the last joiner: macaques combine mimetic rules to optimize their collective decisions

Mechanisms related to collective decision making have recently been found in almost all animal reigns from amoebae to worms, insects and vertebrates, including human beings. Decision-making mechanisms related to collective movements-including pre-departure and joining-have already been studied at different steps of the movement process, but these studies were always carried out separately. We therefore have no understanding of how these different processes are related when they underlie the same collective decision-making event. Here, we consider the whole departure process of two groups of Tonkean macaques (Macaca tonkeana), using a stochastic model. When several exclusive choices are proposed, macaques vote and choose the majority. Individuals then join the movement according to a mimetism based on affiliative relationships. The pre-departure quorum and the joining mimetic mechanism are probably linked, but we have not yet identified which transition mechanism is used. This study shows that decision-making related to macaque group movements is governed by a quorum rule combined with a selective mimetism at departure. This is the first time that transition mechanisms have been described in mammals, which consequently helps understand how a voting process leads to social amplification. Our study also provides the first complete proof that there is continuity in the decision-making processes underlying collective movements in mammals from the first intention movement right through to the last joiner.