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.     

Stop-Signaling Reduces Split Decisions without Impairing Accuracy in the Honeybee Nest-Site Selection Process

In the honeybee swarm nest-site selection process, individual bees gather information about available candidate sites and communicate the information to other bees. The swarm makes an agreement for a candidate site when the number of bees that supports the site reaches a threshold. This threshold is usually referred to as the quorum threshold and it is shown by many studies as a key parameter that is a compromise between the accuracy and speed of decisions. In the present work, we use a model of the honeybee Apis mellifera nest-site selection process to study how the quorum threshold and discovery time of candidate sites have major impact on two unfavorable situations in selecting a nest site: decision deadlock and decision split. We show that cross-inhibitory stop-signaling, delivered among bees supporting different sites, enables swarms to avoid the decision split problem in addition to avoiding the decision deadlock problem that has been previously proposed. We also show that stop-signaling improves decision speed, but compromises decision accuracy in swarms using high quorum thresholds by causing the swarms to be trapped in local optima (e.g., choosing a sub-optimal option that is encountered first). On the other hand, we demonstrate that stop-signaling can reduce split decisions without compromising decision accuracy in swarms using low quorum thresholds when it is compared to the accuracy of swarms using the same threshold values but not exhibiting stop-signaling. Based on our simulations, we suggest that swarms using low quorum thresholds (as well as swarms with large population sizes) would benefit more from exhibiting the stop-signaling activity than not exhibiting it.     

Swarm Cognition: an interdisciplinary approach to?the?study of self-organising biological collectives

Basic elements of cognition have been identified in the behaviour displayed by animal collectives, ranging from honeybee swarms to human societies. For example, an insect swarm is often considered a ??super-organism?? that appears to exhibit cognitive behaviour as a result of the interactions among the individual insects and between the insects and the environment. Progress in disciplines such as neurosciences, cognitive psychology, social ethology and swarm intelligence has allowed researchers to recognise and model the distributed basis of cognition and to draw parallels between the behaviour of social insects and brain dynamics. In this paper, we discuss the theoretical premises and the biological basis of Swarm Cognition, a novel approach to the study of cognition as a distributed self-organising phenomenon, and we point to novel fascinating directions for future work.     

Queen pheromone modulates the expression of epigenetic modifier genes in the brain of honeybee workers

Pheromones are used by many insects to mediate social interactions. In the highly eusocial honeybee (Apis mellifera), queen mandibular pheromone (QMP) is involved in the regulation of the reproductive and other behaviour of workers. The molecular mechanisms by which QMP acts are largely unknown. Here, we investigate how genes responsible for epigenetic modifications to DNA, RNA and histones respond to the presence of QMP in the environment. We show that several of these genes are upregulated in the honeybee brain when workers are exposed to artificial QMP. We propose that pheromonal communication systems, such as those used by social insects, evolved to respond to environmental signals by making use of existing epigenomic machineries.     

Where Next? Group Coordination and Collective Decision Making by Primates

Primate groups need to remain coordinated in their activities and collectively decide when and where to travel if they are to accrue the benefits and minimize the costs of sociality. The achievement of coordinated activity and group decision making therefore has important implications for individual survival and reproduction. The aim of this special issue is to bring together a collection of empirical, theoretical, and commentary articles by primatologists studying this rapidly expanding topic. In this article, we introduce the contributions within the special issue and provide a background to the topic. We begin by focusing on decisions that involve a collective transition between a resting and a moving state, a transition we term making the move. We examine whether specific predeparture behaviors seen during transitions represent intentional processes or more simple response facilitation. Next we classify decisions according to the contribution of individual group members, and describe how, and why, certain individuals can have a disproportionate influence over group-mates?? behavior. We then review how primate groups make decisions on the move. In particular, we focus on how variability in group size and spatial organization helps or hinders information transmission and coordination. We end with a discussion of new tools and methodology that will allow future investigators to address some outstanding questions in primate coordination and decision-making research. We conclude that a better integration of concepts and terminology, along with a focus on how individuals integrate environmental and social information, will be critical to developing a satisfactory understanding of collective patterns of behavior in primate systems.     

Some Work and Some Play: Microscopic and Macroscopic Approaches to Labor and Leisure

Given the option, humans and other animals elect to distribute their time between work and leisure, rather than choosing all of one and none of the other. Traditional accounts of partial allocation have characterised behavior on a macroscopic timescale, reporting and studying the mean times spent in work or leisure. However, averaging over the more microscopic processes that govern choices is known to pose tricky theoretical problems, and also eschews any possibility of direct contact with the neural computations involved. We develop a microscopic framework, formalized as a semi-Markov decision process with possibly stochastic choices, in which subjects approximately maximise their expected returns by making momentary commitments to one or other activity. We show macroscopic utilities that arise from microscopic ones, and demonstrate how facets such as imperfect substitutability can arise in a more straightforward microscopic manner.     

Spatial swarm segregation and reproductive isolation between the molecular forms of Anopheles gambiae

Anopheles gambiae, the major malaria vector in Africa, can be divided into two subgroups based on genetic and ecological criteria. These two subgroups, termed the M and S molecular forms, are believed to be incipient species. Although they display differences in the ecological niches they occupy in the field, they are often sympatric and readily hybridize in the laboratory to produce viable and fertile offspring. Evidence for assortative mating in the field was recently reported, but the underlying mechanisms awaited discovery. We studied swarming behaviour of the molecular forms and investigated the role of swarm segregation in mediating assortative mating. Molecular identification of 1145 males collected from 68 swarms in Donéguébougou, Mali, over 2 years revealed a strict pattern of spatial segregation, resulting in almost exclusively monotypic swarms with respect to molecular form. We found evidence of clustering of swarms composed of individuals of a single molecular form within the village. Tethered M and S females were introduced into natural swarms of the M form to verify the existence of possible mate recognition operating within-swarm. Both M and S females were inseminated regardless of their form under these conditions, suggesting no within-mate recognition. We argue that our results provide evidence that swarm spatial segregation strongly contributes to reproductive isolation between the molecular forms in Mali. However this does not exclude the possibility of additional mate recognition operating across the range distribution of the forms. We discuss the importance of spatial segregation in the context of possible geographic variation in mechanisms of reproductive isolation.     

How many for dinner? Recruitment and monitoring by glances in capuchins

Group members present physical and physiological differences according to their age, sex or social status, which could generate motivation differences among individuals during travel. In spite of these divergences of interest among individuals, the group succeeds more often than not in making a collective decision about departure time and which direction to take. To reach a consensus decision, animals should exchange information relating to characteristics of group movement through different communication channels. The main purpose of this study is to understand the function of behaviour patterns displayed during movements of white-faced capuchins (Cebus capucinus). We designed experiments in which we provoked collective movements involving a binary choice. During experiments, a video camera recorded the behaviour of each capuchin, which enabled us to determine which individuals displayed a behavioural pattern during travel and how this behaviour influenced the other group members. We found that looking backwards seemed to permit the recruitment of group mates during collective movement. This behaviour also seemed to allow the quantification of the number of followers, since the emitter modified its locomotion speed according to this number. In this preliminary study, we showed that visual behaviour was used to recruit and monitor group mates during collective movements and provided information on mechanisms involved in maintaining cohesion and coordination among group members during travel.     

Independence and interdependence in collective decision making: an agent-based model of nest-site choice by honeybee swarms

Condorcet''s jury theorem shows that when the members of a group have noisy but independent information about what is best for the group as a whole, majority decisions tend to outperform dictatorial ones. When voting is supplemented by communication, however, the resulting interdependencies between decision makers can strengthen or undermine this effect: they can facilitate information pooling, but also amplify errors. We consider an intriguing non-human case of independent information pooling combined with communication: the case of nest-site choice by honeybee (Apis mellifera) swarms. It is empirically well documented that when there are different nest sites that vary in quality, the bees usually choose the best one. We develop a new agent-based model of the bees'' decision process and show that its remarkable reliability stems from a particular interplay of independence and interdependence between the bees.     

Proliferation and competition in discrete biological systems

We study the emergence of collective spatio-temporal objects in biological systems by representing individually the elementary interactions between their microscopic components. We use the immune system as a prototype for such interactions. The results of this detailed explicit analysis are compared with the traditional procedure of representing the collective dynamics in terms of densities that obey partial differential equations. The simulations show even for very simple elementary reactions the spontaneous emergence of localized complex structures, from microscopic noise. In turn the effective dynamics of these structures affects the average behaviour of the system in a very decisive way: systems which would according to the differential equations approximation die, display in reality a very lively behaviour. As the optimal modelling method we propose a mixture of microscopic simulation systems describing each reaction separately, and continuous methods describing the average behaviour of the agents.     

Aggregation pattern transitions by slightly varying the attractive/repulsive function

Among collective behaviors of biological swarms and flocks, the attractive/repulsive (A/R) functional links between particles play an important role. By slightly changing the cutoff distance of the A/R function, a drastic transition between two distinct aggregation patterns is observed. More precisely, a large cutoff distance yields a liquid-like aggregation pattern where the particle density decreases monotonously from the inside to the outwards within each aggregated cluster. Conversely, a small cutoff distance produces a crystal-like aggregation pattern where the distance between each pair of neighboring particles remains constant. Significantly, there is an obvious spinodal in the variance curve of the inter-particle distances along the increasing cutoff distances, implying a legible transition pattern between the liquid-like and crystal-like aggregations. This work bridges the aggregation phenomena of physical particles and swarming of organisms in nature upon revealing some common mechanism behind them by slightly varying their inter-individual attractive/repulsive functions, and may find its potential engineering applications, for example, in the formation design of multi-robot systems and unmanned aerial vehicles (UAVs).     

Uncovering the spatial pattern of invasion of the honeybee pest small hive beetle,Aethina tumida,in Italy

The fast tracking of invasion spatial patterns of alien species is crucial for the implementation of preventive and management strategies of those species. Recently, a honeybee pest, the small hive beetle Aethina tumida (hereafter SHB), has been reported in Italy, where it colonized more than 50 apiaries in an area of about 300 km². SHB is a nest parasite and scavenger of honeybee colonies native of Sub-Saharian Africa. Likely being helped by the globalization of apiculture, SHB underwent several invasions in the last twenty years, causing locally relevant economic impact. While many features of its biology have been addressed, an important knowledge gap concerns the spatial invasion dynamics in invaded areas. In this paper we coupled two spatial analysis techniques (geographic profiling and a density-based spatial clustering algorithm) to uncover the possible invasion pattern of SHB in Italy. We identified the port town of Gioia Tauro as the most likely point from which SHB may have spread and suggested the possible successive axes of diffusion. These putative diffusion paths suggest that the SHB spread in south Italy might have been due to a mix of natural dispersal between close apiaries and longer distance movement through faster, likely human-mediated, communication routes.     

Modelling microtubule patterns

The cellular cytoskeleton is well studied in terms of its biological and physical properties, making it an attractive subject for systems approaches. Here, we describe the experimental and theoretical strategies used to study the collective behaviour of microtubules and motors. We illustrate how this led to the beginning of an understanding of dynamic cellular patterns that have precise functions.     

Developmental changes in spatial distribution of in vivo fluorescence and epidermal UV absorbance over Quercus petraea leaves

Background and Aims

Epidermal phenolic compounds (mainly flavonoids) constitute a vital screen that protects the leaf from damage by natural ultraviolet (UV) radiation. The effectiveness of epidermal UV-screening depends on leaf anatomy, the content of UV-screening compounds and their spatial uniformity over the leaf area. To investigate in vivo the spatial pattern of the epidermal UV-screen during leaf development, a fluorescence imaging method was developed to map the epidermal UV-absorbance at a microscopic scale. This study was done on oak (Quercus petraea) leaves that were used as a model of woody dicotyledonous leaves.

Methods

The leaf development of 2-year-old trees, grown outdoors, was monitored, at a macroscopic scale, by in vivo measurements of chlorophyll content per unit area and epidermal UV-absorbance using two optical leaf-clip meters. The distribution of pigments within leaves was assessed in vivo spectroscopically. The microscopic images of UV-induced fluorescence and UV-absorbance acquired in vivo during leaf development were interpreted from spectral characteristics of leaves.

Key Results

At a macroscopic scale, epidermal UV-absorbance was high on the upper leaf side during leaf development, while it increased on the lower leaf side during leaf expansion and reached the adaxial value at maturity. At a microscopic scale, in immature leaves, for both leaf sides, the spatial distribution of epidermal UV-absorbance was heterogeneous, with a pattern depending on the flavonoid content of vacuoles in developing epidermal cells. At maturity, epidermal UV-absorbance was uniform.

Conclusions

The spatial pattern of epidermal UV-screen over the area of oak leaves is related to leaf anatomy during development. In vivo spectroscopy and fluorescence imaging of the leaf surface showed the distribution of pigments within the leaf and hence can provide a tool to monitor optically the leaf development in nature.Key words: Blue-green fluorescence, chlorophyll fluorescence, epidermis, flavonoids, leaf development, microscopic imaging, polyphenols, Quercus petraea     

Selfish-herd behaviour of sheep under threat

Flocking is a striking example of collective behaviour that is found in insect swarms, fish schools and mammal herds [1]. A major factor in the evolution of flocking behaviour is thought to be predation, whereby larger and/or more cohesive groups are better at detecting predators (as, for example, in the 'many eyes theory'), and diluting the effects of predators (as in the 'selfish-herd theory') than are individuals in smaller and/or dispersed groups [2]. The former theory assumes that information (passively or actively transferred) can be disseminated more effectively in larger/cohesive groups, while the latter assumes that there are spatial benefits to individuals in a large group, since individuals can alter their spatial position relative to their group-mates and any potential predator, thus reducing their predation risk [3]. We used global positioning system (GPS) data to characterise the response of a group of 'prey' animals (a flock of sheep) to an approaching 'predator' (a herding dog). Analyses of relative sheep movement trajectories showed that sheep exhibit a strong attraction towards the centre of the flock under threat, a pattern that we could re-create using a simple model. These results support the long-standing assertion that individuals can respond to potential danger by moving towards the centre of a fleeing group [2].