Aggregation in woodlice: social interaction and density effects

Terrestrial isopods are known to be sensitive to humidity, brightness or temperature. Until now, aggregation was assumed to depend on these sensitivities as a result of individual preferences. In this paper, we show that the social component is also important in the isopod aggregation phenomenon. In experimental arenas with two identical shelters up to nearly 90% of woodlice aggregated under shelters. This aggregation was quick as in 10 minutes most of the animals aggregated, irrespective of their density. Nonetheless, 10-15% of the animals walked around the arena, rarely forming very small and short-lasting aggregates outside shelters. Woodlice aggregated preferably under one of the shelters in 77% of experiments. Indeed, almost 80% of the animals out of 40, 60 or 80 animals in the arena aggregated under one shelter. In arenas with 100 individuals the aggregations were proportionally smaller (70%). Our results revealed that 70 animals was a maximum number of woodlice in an aggregate. We concluded that the location of aggregates is strongly governed by individual preferences but the dynamics of aggregation and collective choice are controlled by social interaction between congeners. The tested densities of the animals in the arena did not impact the aggregation patterns.     

Scalable rules for coherent group motion in a gregarious vertebrate

Individuals of gregarious species that initiate collective movement require mechanisms of cohesion in order to maintain advantages of group living. One fundamental question in the study of collective movement is what individual rules are employed when making movement decisions. Previous studies have revealed that group movements often depend on social interactions among individual members and specifically that collective decisions to move often follow a quorum-like response. However, these studies either did not quantify the response function at the individual scale (but rather tested hypotheses based on group-level behaviours), or they used a single group size and did not demonstrate which social stimuli influence the individual decision-making process. One challenge in the study of collective movement has been to discriminate between a common response to an external stimulus and the synchronization of behaviours resulting from social interactions. Here we discriminate between these two mechanisms by triggering the departure of one trained Merino sheep (Ovis aries) from groups containing one, three, five and seven naïve individuals. Each individual was thus exposed to various combinations of already-departed and non-departed individuals, depending on its rank of departure. To investigate which individual mechanisms are involved in maintaining group cohesion under conditions of leadership, we quantified the temporal dynamic of response at the individual scale. We found that individuals'' decisions to move do not follow a quorum response but rather follow a rule based on a double mimetic effect: attraction to already-departed individuals and attraction to non-departed individuals. This rule is shown to be in agreement with an adaptive strategy that is inherently scalable as a function of group size.     

Interspecific shared collective decision-making in two forensically important species

To date, the study of collective behaviour has mainly focused on intraspecific situations: the collective decision-making of mixed-species groups involving interspecific aggregation–segregation has received little attention. Here, we show that, in both conspecific and heterospecific groups, the larvae of two species (Lucilia sericata and Calliphora vomitoria, calliphorid carrion-feeding flies) were able to make a collective choice. In all groups, the choice was made within a few minutes and persisted throughout the period of the experiment. The monitoring of a focal individual within a group showed that these aggregations were governed by attractive and retentive effects of the group. Furthermore, the similarity observed between the conspecific and heterospecific groups suggested the existence of shared aggregation signals. The group size was found to have a stronger influence than the species of necrophagous larvae. These results should be viewed in relation to the well-known correlation between group size and heat generation. This study provides the first experimental examination of the dynamics of collective decision-making in mixed-species groups of invertebrates, contributing to our understanding of the cooperation–competition phenomenon in animal social groups.     

Individual discrimination capability and collective decision-making

Amplification is the main component of many collective phenomena in social and gregarious insects. In a society, individuals face a mixed palette of odours coming from different groups (lines, strains) and individuals present discrimination capabilities. However, often at the collective level, different groups may cooperate and act together. To understand this apparent contradiction, we use a model of food recruitment where each group of foragers have its own blend of pheromone trail that is partly recognized by the others groups. The model shows that a low level of recognition between signals is sufficient to produce a collaborative pattern between groups and that beyond a critical value of recognition, only the aggregation of all the groups around the same food source is observed. The comparison between this model and one describing the site selection by gregarious insects (e.g. cockroach) suggests that such collective response is a generic property of social phenomena governed by amplification processes.     

The impact of individual perceptual and cognitive factors on collective states in a data-driven fish school model

In moving animal groups, social interactions play a key role in the ability of individuals to achieve coordinated motion. However, a large number of environmental and cognitive factors are able to modulate the expression of these interactions and the characteristics of the collective movements that result from these interactions. Here, we use a data-driven fish school model to quantitatively investigate the impact of perceptual and cognitive factors on coordination and collective swimming patterns. The model describes the interactions involved in the coordination of burst-and-coast swimming in groups of Hemigrammus rhodostomus. We perform a comprehensive investigation of the respective impacts of two interactions strategies between fish based on the selection of the most or the two most influential neighbors, of the range and intensity of social interactions, of the intensity of individual random behavioral fluctuations, and of the group size, on the ability of groups of fish to coordinate their movements. We find that fish are able to coordinate their movements when they interact with their most or two most influential neighbors, provided that a minimal level of attraction between fish exist to maintain group cohesion. A minimal level of alignment is also required to allow the formation of schooling and milling. However, increasing the strength of social interactions does not necessarily enhance group cohesion and coordination. When attraction and alignment strengths are too high, or when the heading random fluctuations are too large, schooling and milling can no longer be maintained and the school switches to a swarming phase. Increasing the interaction range between fish has a similar impact on collective dynamics as increasing the strengths of attraction and alignment. Finally, we find that coordination and schooling occurs for a wider range of attraction and alignment strength in small group sizes.     

Benefits of aggregation in woodlice: a factor in the terrestrialization process?

In the animal kingdom, living in group is driven by a tradeoff between the costs and the benefits of this way of life. This review focuses especially on the benefits of aggregation and crowding in woodlice (Crustacea: Isopoda: Oniscidea). Indeed, woodlice are well known to live in groups. Their aggregation behavior, as described in the early works of Allee, is regarded as a mechanism to prevent desiccation to which woodlice are extremely sensitive. However, it is now clear that there are additional benefits to aggregation in woodlice. Hence, this review addresses not only the limitation of water loss as the main factor explaining aggregation patterns, but also alternative explanations as reduction of oxygen consumption, increase in body growth, biotic stimuli for reproduction, better access to mates, possible shared defenses against predators, promotion of coprophagy as a secondary food source, sheltering behavior and the acquisition of internal symbionts. In addition, we place woodlice in the context of a terrestrialization process and propose that woodlice—the only suborder of Crustacea almost entirely composed of strictly terrestrial species—are a model taxon for studying the evolution of sociality through the transition from water to land. Further, we discuss other ultimate causes of aggregation preserved in terrestrial isopods in light of those explained in aquatic isopods and under the concept of exaptation. This knowledge could help understand, in this and other taxa, how the spatial closeness between conspecifics may promote the colonization of new environments and nonphysiological responses to climatic constraints.     

Has Predation Shaped the Social Systems of Arboreal Primates?

I studied antipredator behavior in two species of monkeys to elucidate the role of predation in shaping the social systems of arboreal primates. I compared the responses of monkeys to auditory and visual contact with predators to response elicited by sound playback experiments using the recorded calls of predators. Changes in vigilance and aggregation persisting up to 30 min after predator encounter occurred in both cases. Measures of vigilance shed light on individual perceptions of risk, while aggregation measures—intragroup spatial cohesion and polyspecific associations—permit direct inference about the protective benefits of grouping for the monkeys. They responded to real predator encounters and simulations in similar ways. Thus, sound playbacks of predator vocalizations are effective to simulate predator proximity. Contrary to predictions, predator encounters did not lead invariably to increased cohesion within groups or to increased time spent vigilant. Moreover, behavior in polyspecific associations was no different from that in single-species groups. Only red colobus encountering chimpanzees behaved as predicted by increasing vigilance and intragroup cohesion. The red colobus social system may have developed to protect against chimpanzee attack. In contrast, red-tailed monkey encounters with raptors and chimpanzees involved no change in time spent vigilant, coupled with decreases in intragroup cohesion. I conclude that predation is not a uniform selective pressure and patterns of social behavior within groups do not predict antipredator behavior.     

Effects of group size on aggregation against desiccation in woodlice (Isopoda: Oniscidea)

Aggregation in terrestrial isopods, a behaviour that results in the formation of dense clusters, is readily accepted as a mechanism of resistance to desiccation. Thus, aggregation is considered to be an adaptation to terrestrial life in this fully terrestrial suborder of crustaceans. In the present study of Porcellio scaber Latreille, a cosmopolitan species, individual water loss is investigated experimentally as a function of the size of the aggregates and, for the first time, over a large range of group sizes (groups of 1, 10, 20, 40, 60, 80 and 100 individuals). From the perspective of an isolated individual, aggregation behaviour is effective in reducing the rate of water loss whatever the group size, and reduces the individual water loss rate by more than half in large groups. However, the water loss rate of an individual follows a power law according to group size. Accordingly, if the addition of individuals to small groups strongly reduces the water losses per individual, adding individuals to large groups only slightly reduces the individual water losses. Thus, the successful reduction of the water loss rate by this aggregation behaviour is confirmed, although only up to a certain limit, particularly if the number of individuals per aggregate exceeds 50–60 under the experimental conditions used in the present study. Moreover, the individual surface area exposed to the air, as a function of group size, follows a similar pattern (i.e. a similar power law). Thus, a geometrical explanation is proposed for the nonlinear water losses in woodlice aggregates. These results are discussed in relation to the group sizes observed both in the laboratory and the field.     

Social aggregation of the marine isopod Cirolana harfordi does not rely on the availability of light‐reducing shelters

Social aggregation under shelters can afford benefits to animals such as protection from predators. Many isopods and insects are negatively phototactic and this may help them gravitate towards shelter. Previous studies show that, when placed in an arena with two red shelters, specimens of the marine isopod Cirolana harfordi and the terrestrial isopod Porcelio scaber pick one of the two shelters at random and aggregate under it, demonstrating social aggregation under light‐reducing shelters. In the present study, an arena with two clear shelters was used to determine whether group sizes of 4, 8, 12 and 16 C. harfordi specimens display social aggregation when the shelters do not accommodate negative phototaxis. In all group sizes, C. harfordi specimens picked one of the shelters at random and significantly more animals aggregated under this shelter compared with the other. Cirolana harfordi also displayed aggregation in an arena with no shelters. Accordingly, C. harfordi specimens do not require shelters that reduce light to display social aggregation. The ability to locate suitable shelter under which there is no substantial reduction in light could benefit the animal in a natural environment comprising heavily shaded areas, as well as at night.     

Complex Dynamics Based on a Quorum: Decision-Making Process by Cockroaches in a Patchy Environment

In the absence of complex communication and a global knowledge of the environment, cockroaches are able to assess the availability of resources and to reach a consensual decision: the group aggregates in a single resting site. We show that the aggregation dynamics and the collective shelter selection of cockroaches are influenced by their social context as, unlike single individuals, groups of cockroaches are more likely to respond to environmental heterogeneities. The decision of individuals to stay under a shelter relies on the modulation of their resting time, according to the perception of two local cues: (1) the shelters luminosity and (2) the number of congeners. This study on the cockroach species Periplaneta americana highlights a shelter-selection mechanism based on an amplification process resulting from the interactions between congeners. This mechanism leads to complex spatiotemporal aggregation dynamics characterized by transient bimodality, bifurcation patterns (shelter selection) and the existence of a quorum size in the settlement behaviour of the cockroaches. Finally, we discuss the generic aspect for other gregarious species of the collective decision-making process demonstrated for cockroaches.     

Always together: mate guarding or predator avoidance as determinants of group cohesion in white‐breasted mesites?

Being a member of a cohesive group can have fitness benefits such as decreased predation risk, increased feeding efficiency as well as enhanced access to social information and mates. However, competition and the risk of parasite transmission exert centrifugal forces on group‐living. Thus, the actual degree of cohesion is expected to vary as a function of the relative importance of several social and ecological factors. White‐breasted mesites Mesitornis variegata are medium‐sized ground‐dwelling birds endemic to the dry deciduous forests of western Madagascar. They live in stable breeding pairs or small family groups, mate monogamously and often form temporary heterospecific associations with canopy‐dwelling bird species that give alarm calls to which mesites respond with anti‐predator behaviours. We investigated the potential effects of predation risk and mate defence on mesite group cohesion by analysing inter‐individual distances of 20 groups as a function of mesite social organization, alarm call events, the size of associated heterospecific flocks, and the adults' reproductive state. Mesite social units were very cohesive, particularly in families, when associated with smaller heterospecific flocks, and after an alarm call event. Adult reproductive state did not influence breeding partners' cohesion. Therefore, the pronounced group cohesion in mesites seems to be mainly a response to the high predation risk typically associated with a terrestrial life‐style, and not to mate‐guarding. However, we suggest that high group cohesion due to predation risk could limit opportunities for solitary extra‐territorial forays to obtain extra‐pair copulations, thereby contributing to a strictly monogamous system in this species.     

Social Relationships among Males in Multimale Siamang Groups

I quantified social and spatial interactions among adults in 4 multimale siamang (Symphalangus syndactylus) groups to evaluate the importance of aggression and avoidance in mediating male-male relationships. Actual genetic relationships among adults are unknown, but available mitochondrial data suggest that in 3 of 4 groups, neither male was the offspring or maternal sibling of the female, whereas in the fourth group, a matrilineal relationship between the female and 1 adult male was not excluded. Rates of aggression involving male-male dyads were very low. One male-female dyad maintained closer spatial cohesion than those of other adult dyads in 3 of 4 groups. Nonetheless, all adult males spent substantial percentages of their time ≤20 m from other adults in their groups. The percentages of time that male-male dyads spent in social grooming interactions did not differ from those of male-female dyads. In 3 groups, both males copulated with the group female. While previous studies have reported high rates of aggression between adult males and subadult male group members in siamangs, my results suggest that male-male relationships in multimale groups at Way Canguk were relatively harmonious. Acceptance of multimale grouping (and in some cases sexual polyandry) suggests that the benefits outweigh the costs under some circumstances. If there was a genetic relationship between males, then tolerance of delayed dispersal and copulation with the adult female may function as a form of parental investment. Males may also benefit from multimale grouping via enhanced territorial defense or reduced costs of mate defense.     

Moving together: Incidental leaders and naïve followers

Elucidating whether common general mechanisms govern collective movements in a wide range of species is a central issue in the study of social behaviour. In this paper, we describe a new experimental paradigm for studying the dynamic of collective movements. Some sheep (Ovis aries) were first trained to move towards a coloured panel, in response to a sound cue. We present data comparing the behaviour of test groups composed of one of the trained sheep and 3 naïve sheep, and control groups composed of 4 naïve sheep. In the tests, for both test and control groups, sheep were observed for 20 min before the sound cue was delivered and the panel made visible. Before the sound, trained and naïve sheep were similar in terms of activity budgets, spatial distribution, social behaviour and spontaneous movement initiation. After the sound, trained sheep moved toward the panel and systematically triggered a collective movement in all test groups. The results suggest that any individual moving away from the group can elicit a collective movement. Our experimental protocol provides an opportunity to quantify mechanisms involved in group movements, and to investigate differences between species and the effect of social context on collective decision-making.     

Oosorption and oocyte loss in a terrestrial isopod under stressful conditions

An increased number of resorbed oocytes was observed in ovaries of terrestrial isopods which were kept under different experimental temperature and photophase regimes compared with those observed in the natural population. Regardless of the nature of the stimulus: high or low temperature or long and short photophases, the female always responded through oosorption. In an iteroparous species such as Porcellio ficulneus B.-L., recruitment of resources for future utilization could be its main response to adverse ambient conditions.     

The principles of collective animal behaviour

In recent years, the concept of self-organization has been used to understand collective behaviour of animals. The central tenet of self-organization is that simple repeated interactions between individuals can produce complex adaptive patterns at the level of the group. Inspiration comes from patterns seen in physical systems, such as spiralling chemical waves, which arise without complexity at the level of the individual units of which the system is composed. The suggestion is that biological structures such as termite mounds, ant trail networks and even human crowds can be explained in terms of repeated interactions between the animals and their environment, without invoking individual complexity. Here, I review cases in which the self-organization approach has been successful in explaining collective behaviour of animal groups and societies. Ant pheromone trail networks, aggregation of cockroaches, the applause of opera audiences and the migration of fish schools have all been accurately described in terms of individuals following simple sets of rules. Unlike the simple units composing physical systems, however, animals are themselves complex entities, and other examples of collective behaviour, such as honey bee foraging with its myriad of dance signals and behavioural cues, cannot be fully understood in terms of simple individuals alone. I argue that the key to understanding collective behaviour lies in identifying the principles of the behavioural algorithms followed by individual animals and of how information flows between the animals. These principles, such as positive feedback, response thresholds and individual integrity, are repeatedly observed in very different animal societies. The future of collective behaviour research lies in classifying these principles, establishing the properties they produce at a group level and asking why they have evolved in so many different and distinct natural systems. Ultimately, this research could inform not only our understanding of animal societies, but also the principles by which we organize our own society.     

Grooming-at-a-distance by exchanging calls in non-human primates

The ‘social bonding hypothesis'' predicts that, in large social groups, functions of gestural grooming should be partially transferred to vocal interactions. Hence, vocal exchanges would have evolved in primates to play the role of grooming-at-a-distance in order to facilitate the maintenance of social cohesion. However, there are few empirical studies testing this hypothesis. To address this point, we compared the rate of contact call exchanges between females in two captive groups of Japanese macaques as a function of female age, dominance rank, genetic relatedness and social affinity measured by spatial proximity and grooming interactions. We found a significant positive relationship between the time spent on grooming by two females and the frequency with which they exchanged calls. Our results conform to the predictions of the social bonding hypothesis, i.e. vocal exchanges can be interpreted as grooming-at-a-distance.     

When is bigger better? The effects of group size on the evolution of helping behaviours

Understanding the evolution of sociality in humans and other species requires understanding how selection on social behaviour varies with group size. However, the effects of group size are frequently obscured in the theoretical literature, which often makes assumptions that are at odds with empirical findings. In particular, mechanisms are suggested as supporting large‐scale cooperation when they would in fact rapidly become ineffective with increasing group size. Here we review the literature on the evolution of helping behaviours (cooperation and altruism), and frame it using a simple synthetic model that allows us to delineate how the three main components of the selection pressure on helping must vary with increasing group size. The first component is the marginal benefit of helping to group members, which determines both direct fitness benefits to the actor and indirect fitness benefits to recipients. While this is often assumed to be independent of group size, marginal benefits are in practice likely to be maximal at intermediate group sizes for many types of collective action problems, and will eventually become very small in large groups due to the law of decreasing marginal returns. The second component is the response of social partners on the past play of an actor, which underlies conditional behaviour under repeated social interactions. We argue that under realistic conditions on the transmission of information in a population, this response on past play decreases rapidly with increasing group size so that reciprocity alone (whether direct, indirect, or generalised) cannot sustain cooperation in very large groups. The final component is the relatedness between actor and recipient, which, according to the rules of inheritance, again decreases rapidly with increasing group size. These results explain why helping behaviours in very large social groups are limited to cases where the number of reproducing individuals is small, as in social insects, or where there are social institutions that can promote (possibly through sanctioning) large‐scale cooperation, as in human societies. Finally, we discuss how individually devised institutions can foster the transition from small‐scale to large‐scale cooperative groups in human evolution.     

Exploring How a Shift in the Physical Environment Shapes Individual and Group Behavior across Two Social Contexts

The presence or absence of social counterparts can be instrumental in shaping both individual and collective behaviors. Furthermore, factors of the social environment may safeguard individuals from environmental stressors. In the study reported here, we tested the effects of moving into a new habitat on the mean, variance, and repeatability of individual behavioral tendencies between two social contexts (isolated vs. in a social group). Using the arid social spider, Stegodyphus dumicola (Araneae: Eresidae), we tested whether individuals' boldness was influenced by either (i) their time spent in a social group or (ii) their latency since having moved into a new habitat. We found that the effect of moving into a new habitat on individuals' boldness depended on whether spiders entered the novel environment in isolation or as part of a social group. Spiders that experienced a habitat shift with a social group showed no change in their average boldness, whereas individuals that shifted environments in isolation showed an increase in their mean boldness. Interestingly, neither of these trends was influenced by the time which had elapsed since the habitat shift, suggesting that shifting habitats has a lasting effect on isolated spiders' behavioral tendencies. Finally, we assessed how time spent in a new environment influenced colonies' collective foraging behavior. Here, we found that the longer social groups remained in a new environment, the faster the group responded to prey. Taken together, our data demonstrate that the effects of shifting physical environments on individuals' boldness may depend on individuals' social context, and that group tenure is associated with subtle shifts in colonies' collective foraging behavior.     

An evolutionary timescale for terrestrial isopods and a lack of molecular support for the monophyly of Oniscidea (Crustacea: Isopoda)

The marine metazoan fauna first diversified in the early Cambrian, but terrestrial environments were not colonized until at least 100 million years later. Among the groups of organisms that successfully colonized land is the crustacean order Isopoda. Of the 10,000 described isopod species, ~ 3,600 species from the suborder Oniscidea are terrestrial. Although it is widely thought that isopods colonized land only once, some studies have failed to confirm the monophyly of Oniscidea. To infer the evolutionary relationships among isopod lineages, we conducted phylogenetic analyses of nuclear 18S and 28S and mitochondrial COI genes using maximum-likelihood and Bayesian methods. We also analyzed a second data set comprising all of the mitochondrial protein-coding genes from a smaller sample of isopod taxa. Based on our analyses using a relaxed molecular clock, we dated the origin of terrestrial isopods at 289.5 million years ago (95% credibility interval 219.6–358.9 million years ago). These predate the known fossil record of these taxa and coincide with the formation of the supercontinent Pangaea and with the diversification of vascular plants on land. Our results suggest that the terrestrial environment has been colonized more than once by isopods. The monophyly of the suborder Oniscidea was not supported in any of our analyses, conflicting with classical views based on morphology. This draws attention to the need for further work on this group of isopods.     

Collective arousal when reuniting after temporary separation in Tonkean macaques

Celebrations and bursts of communal joy can occur spontaneously in human communities based on mechanisms of emotional contagion. Some examples of similar collective excitement have been reported in animals when they reunite or anticipate rewards, but little is known about the processes and meaning of these multiple interactions. We experimentally studied such collective arousals in two captive groups of Tonkean macaques (Macaca tonkeana) within the context of reunions following the temporary separation of two subgroups. We compared the behaviors of individuals after separation periods of 2 and 48 h with a control period with no separation. This study showed that it is possible to reproducibly induce bursts of friendly interactions in which groupmates run around over a period of several minutes, embracing and grasping one another while displaying numerous affiliative vocalizations and facial expressions. The longer the period of separation, the higher and longer-lasting the rates of affiliative interactions were. Individuals affiliated more frequently with groupmates from a previously separated subgroup than with those having stayed in their own subgroup. Collective arousal was followed by a quieter period characterized by high rates of contact-sitting and social grooming. These results point at the role of collective arousals in social cohesion; they could resolve social tension and renew social relationships. We propose that the emotional state experienced by Tonkean macaques during such events represents a disposition similar to that giving rise to what we humans call "shared joy."