Emergence and retention of a collective memory in cockroaches.

The stability of collective decisions-making in social systems is crucial as it can lead to counterintuitive phenomena such as collective memories, where an initial choice is challenged by environmental changes. Many social species face the challenge to perform collective decisions under variable conditions. In this study, we focused on situations where isolated individuals and groups of the American cockroach (Periplaneta americana) had to choose between two shelters with different luminosities that were inverted during the experiment. The darker shelter was initially preferred, but only groups that reached a consensus within that shelter maintain their choice after the light inversion, while isolated individuals and small groups lacked site fidelity. Our mathematical model, incorporating deterministic and probabilistic elements, sheds light on the significance interactions and their stochasticity in the emergence and retention of a collective memory.

A Data-Driven Simulation of the Trophallactic Network and Intranidal Food Flow Dissemination in Ants.

Food sharing can occur in both social and non-social species, but it is crucial in eusocial species, in which only some group members collect food. This food collection and the intranidal (i.e., inside the nest) food distribution through trophallactic (i.e., mouth-to-mouth) exchanges are fundamental in eusocial insects. However, the behavioural rules underlying the regulation and the dynamics of food intake and the resulting networks of exchange are poorly understood. In this study, we provide new insights into the behavioural rules underlying the structure of trophallactic networks and food dissemination dynamics within the colony. We build a simple data-driven model that implements interindividual variability and the division of labour to investigate the processes of food accumulation/dissemination inside the nest, both at the individual and collective levels. We also test the alternative hypotheses (no variability and no division of labour). The division of labour, combined with inter-individual variability, leads to predictions of the food dynamics and exchange networks that run, contrary to the other models. Our results suggest a link between the interindividual heterogeneity of the trophallactic behaviours, the food flow dynamics and the network of trophallactic events. Our results show that a slight level of heterogeneity in the number of trophallactic events is enough to generate the properties of the experimental networks and seems to be crucial for the creation of efficient trophallactic networks. Despite the relative simplicity of the model rules, efficient trophallactic networks may emerge as the networks observed in ants, leading to a better understanding of the evolution of self-organisation in such societies.

Differential Gene Expression Correlates with Behavioural Polymorphism during Collective Behaviour in Cockroaches.

Consistent inter-individual variation in the propensity to perform different tasks (animal personality) can contribute significantly to the success of group-living organisms. The distribution of different personalities in a group influences collective actions and therefore how these organisms interact with their environment. However, we have little understanding of the proximate mechanisms underlying animal personality in animal groups, and research on this theme has often been biased towards organisms with advanced social systems. The goal of this study is to investigate the mechanistic basis for personality variation during collective behaviour in a species with rudimentary societies: the American cockroach. We thus use an approach which combines experimental classification of individuals into behavioural phenotypes ('bold' and 'shy' individuals) with comparative gene expression. Our analyses reveal differences in gene expression between behavioural phenotypes and suggest that social context may modulate gene expression related to bold/shy characteristics. We also discuss how cockroaches could be a valuable model for the study of genetic mechanisms underlying the early steps in the evolution of social behaviour and social complexity. This study provides a first step towards a better understanding of the molecular mechanisms associated with differences in boldness and behavioural plasticity in these organisms.

Does a high social status confer greater levels of trust from groupmates? An experimental study of leadership in domestic horses.

In collective movements, specific individuals may emerge as leaders. In this study on the domestic horse (Equus ferus caballus), we conducted experiments to establish if an individual is successfully followed due to its social status (including hierarchical rank and centrality). We first informed one horse about a hidden food location and recorded by how many it was followed when going back to this location. In this context, all horses lead their groupmates successfully. In a second step, we tested whether group members would trust some leaders more than others by removing the food before the informed individual led the group back to the food location. In addition, two control initiators with intermediate social status for which the food was not removed were tested. The results, confirmed by simulations, demonstrated that the proportions of followers for the unreliable initiator with highest social status are greater than the ones of the unreliable initiator with lowest social status. Our results suggest an existing relationship between having a high social status and a leadership role. Indeed, the status of a leader sometimes prevail at the detriment of the accuracy of the information, because an elevated social status apparently confers a high level of trust.

Schooling in habitats with aggregative sites: The case of tropical tuna and floating objects.

Many marine and terrestrial species live in groups, whose sizes and dynamics can vary depending on the type and strength of their social interactions. Typical examples of such groups in vertebrates are schools of fish or flocks of bird. Natural habitats can encompass a wide range of spatial heterogeneities, which can also shape the structure of animal groups, depending on the interplay between the attraction/repulsion of environmental cues and social interactions. A key issue in modern applied ecology and conservation is the need to understand the relationship between these ethological and ecological scales in order to account for the social behaviour of animals in their natural environments. Here, we introduce a modeling approach which studies animal groups within heterogeneous habitats constituted by a set of aggregative sites. The model properties are investigated considering the case study of tropical tuna schools and their associative behavior with floating objects, a question of global concern, given the thousands of floating objects deployed by industrial tropical tuna fisheries worldwide. The effects of increasing numbers of aggregative sites (floating objects) on tuna schools are studied. This study offers a general modeling framework to study social species in their habitats, accounting for both ethological and ecological drivers of animal group dynamics.

The effect of idiosyncrasy on aggregation in group-living organisms.

We use a minimalistic mathematical model with a limited number of parameters to evaluate the impact of interindividual differences in the collective decision-making of a group. As it turns out, in most cases, heterogeneous groups are more efficient in their decision-making than homogenous ones, especially when considering small group sizes. In reality, being different disfavours the emergence of an hysteresis and a collective threshold which are characteristics of such cooperative species while keeping inter-attractions the same between individuals. Finally, when the cooperativity becomes very large, we observe an explosion of accessible stable states.

Consensus driven by a minority in heterogenous groups of the cockroach Periplaneta american a.

Many social species are able to perform collective decisions and reach consensus. However, how the interplay between social interactions, the diversity of preferences among the group members and the group size affects these dynamics is usually overlooked. The collective choice between odourous and odorless shelters is tested for the following three groups of social cockroaches (Periplaneta americana) which are solitary foragers: naive (individuals preferring the odorous shelter), conditioned (individuals without preference), and mixed (combining, unevenly, conditioned, and naive individuals). The robustness of the consensus is not affected by the naive individuals' proportion, but the rate and the frequency of selection of the odorous shelter are correlated to this proportion. In mixed groups, the naive individuals act as influencers. Simulations based on the mechanisms highlighted in our experiments predict that the consensus emerges only for intermediate group sizes. The universality of these mechanisms suggests that such phenomena are widely present in social systems.

Variation in personality can substitute for social feedback in coordinated animal movements.

Collective movements are essential for the effective function of animal societies, but are complicated by the need for consensus among group members. Consensus is typically assumed to arise via feedback mechanisms, but this ignores inter-individual variation in behavioural tendency ('personality'), which is known to underpin the successful function of many complex societies. In this study, we use a theoretical approach to examine the relative importance of personality and feedback in the emergence of collective movement decisions in animal groups. Our results show that variation in personality dramatically influences collective decisions and can partially or completely replace feedback depending on the directionality of relationships among individuals. The influence of personality increases with the exaggeration of differences among individuals. While it is likely that both feedback and personality interact in nature, our findings highlight the potential importance of personality in driving collective processes.

Hierarchical networks of food exchange in the black garden ant Lasius niger.

In most eusocial insects, the division of labor results in relatively few individuals foraging for the entire colony. Thus, the survival of the colony depends on its efficiency in meeting the nutritional needs of all its members. Here, we characterize the network topology of a eusocial insect to understand the role and centrality of each caste in this network during the process of food dissemination. We constructed trophallaxis networks from 34 food-exchange experiments in black garden ants (Lasius niger). We tested the influence of brood and colony size on (i) global indices at the network level (i.e., efficiency, resilience, centralization, and modularity) and (ii) individual values (i.e., degree, strength, betweenness, and the clustering coefficient). Network resilience, the ratio between global efficiency and centralization, was stable with colony size but increased in the presence of broods, presumably in response to the nutritional needs of larvae. Individual metrics highlighted the major role of foragers in food dissemination. In addition, a hierarchical clustering analysis suggested that some domestics acted as intermediaries between foragers and other domestics. Networks appeared to be hierarchical rather than random or centralized exclusively around foragers. Finally, our results suggested that networks emerging from social insect interactions can improve group performance and thus colony fitness.

Effects of habitat modifications on the movement behavior of animals: the case study of Fish Aggregating Devices (FADs) and tropical tunas.

BACKGROUND: Aggregation sites represent important sources of environmental heterogeneity and can modify the movement behavior of animals. When these sites are artificially established through anthropogenic actions, the consequent alterations to animal movements may impact their ecology with potential implications for their fitness. Floating objects represent important sources of habitat heterogeneity for tropical tunas, beneath which these species naturally aggregate in large numbers. Man-made floating objects, called Fish Aggregating Devices (FAD), are used by fishers on a massive scale to facilitate fishing operations. In addition to the direct impacts that fishing with FADs has on tuna populations, assessing the effects of increasing the numbers of FADs on the ecology of tuna is key for generating sound management and conservation measures. METHODS: This study investigates the effects of increasing numbers of FADs (aggregation sites) on the movements of tunas, through the comparison of electronic tagging data recorded from 146 individuals tunas (yellowfin tuna, Thunnus albacares, and skipjack tuna, Katsuwonus pelamis) tagged in three instrumented anchored FAD arrays (Mauritius, Oahu-Hawaii and Maldives), that differed according to their distances among neighboring FADs. The effect of increasing inter-FAD distances is studied considering a set of indices (residence times at FADs and absence (travel) times between two visits at FADs) and their trends. RESULTS: When inter-FAD distances decrease, tuna visit more FADs (higher connectivity between FADs), spend less time travelling between FADs and more time associated with them. The trends observed for the absence (travel) times appear to be compatible with a random-search component in the movement behaviour of tunas. Conversely, FAD residence times showed opposite trends, which could be a result of social behavior and/or prey availability. CONCLUSION: Our results provide the first evidence of changes in tuna associative behavior for increasing FAD densities. More generally, they highlight the need for comparing animal movements in heterogeneous habitats in order to improve understanding of the impacts of anthropogenic habitat modifications on the ecology of wild animals.

A methodological framework for characterizing fish swimming and escapement behaviors in trawls.

Knowledge about fish behavior is crucial to be able to influence the capture process and catch species composition. The rapid expansion of the use of underwater cameras has facilitated unprecedented opportunities for studying the behavior of species interacting with fishing gears in their natural environment. This technological advance would greatly benefit from the parallel development of dedicated methodologies accounting for right-censored observations and variable observation periods between individuals related to instrumental, environmental and behavioral events. In this paper we proposed a methodological framework, based on a parametric Weibull mixture model, to describe the process of escapement attempts through time, test effects of covariates and estimate the probability that a fish will attempt to escape. We additionally proposed to better examine the escapement process at the individual level with regard to the temporal dynamics of escapement over time. Our approach was used to analyze gadoids swimming and escapement behaviors collected using a video set up in front of a selective device known to improve selectivity on gadoids in the extension of a bottom trawl. Comparison of the fit of models indicates that i) the instantaneous rate of escape attempts is constant over time and that the escapement process can be modelled using an exponential law; ii) the mean time before attempting to escape increases with the increasing number of attempts; iii) more than 80% of the gadoids attempted to escape through the selective device; and iv) the estimated probability of success was around 15%. Effects of covariates on the probability of success were investigated using binomial regression but none of them were significant. The data set collected is insufficient to make general statements, and further observations are required to properly investigate the effect of intrinsic and extrinsic factors governing gadoids behavior in trawls. This methodology could be used to better characterize the underlying behavioral process of fish in other parts of a bottom trawl or in relation to other fishing gears.

Colony co-founding in ants is an active process by queens.

Cooperative breeding may be selected for in animals when, on average, it confers greater benefits than solitary breeding. In a number of eusocial insects (i.e., ants, bees, wasps, and termites), queens join together to co-create new nests, a phenomenon known as colony co-founding. It has been hypothesised that co-founding evolved because queens obtain several fitness benefits. However, in ants, previous work has suggested that co-founding is a random process that results from high queen density and low nest-site availability. We experimentally examined nest-founding behaviour in the black garden ant, Lasius niger. We gave newly mated queens the choice between two empty nesting chambers, and compared their distribution across the two chambers with that expected under random allocation. We found that queens formed associations of various sizes; in most instances, queens group together in a single chamber. Across all experiments, the frequency of larger groups of queens was significantly higher than expected given random assortment. These results indicate colony co-founding in ants may actually be an active process resulting from mutual attraction among queens. That said, under natural conditions, ecological constraints may limit encounters among newly mated queens.

Modelling persistence over generations in biological and cultural evolution based on differential paces of change.

Paces of change are faster in cultural evolution than in biological evolution due to different levels of stability in information storage. This study develops mathematical models to investigate the consequences of differential mutation rates on the ability of groups of information units to survive over many generations. We examined the ability of groups composed of connected units to live on despite the occurrence of deleterious mutations that occur at probabilities ranging from 10-1 to 10-6. It appears that the degree of connection between units should be high enough for groups to persist across generations, but this alone did not ensure their survival; when groups of units were limited in size and subjected to high mutation rates, they did not survive for very long. By contrast, a significant proportion of groups were able to survive numerous generations if mutation rates were low and/or group size was large. The results revealed that the mean number of surviving generations was minimized for certain sizes of groups. When allowing information units to duplicate at each generation, simulation showed that a great number of groups avoided extinction even when mutating at the rate of cultural change if the initial group size was large and the duplication rate was high enough to counteract the consequences of environmental perturbations. The modelling described in this study sets out the conditions under which groups of units can survive along generations. It should serve as a basis for further investigations about the links between processes of biological and cultural changes.

Alteration of the aggregation and spatial organization of the vector of Chagas disease, Triatoma infestans, by the parasite Trypanosoma cruzi.

Triatominae insects are vectors of the parasite Trypanosoma cruzi, the etiological agent of Chagas disease affecting millions of people in Latin America. Some species, such as Triatoma infestans, live in the human neighborhood, aggregating in walls or roof cracks during the day and going out to feed blood at night. The comprehension of how sex and T. cruzi infection affect their aggregation and geotaxis is essential for understanding their spatial organization and the parasite dispersion. Experiments in laboratory-controlled conditions were carried out with groups of ten adults of T. infestans able to explore and aggregate on a vertical surface. The influence of the sex (male vs. female) and the proportion of infected insects in the group were tested (100% of infected insects vs. a small proportion of infected insects, named infected and potentially weakly infected groups, respectively). Therefore, four distinct groups of insects were tested: infected males, infected females, potentially weakly infected males, and potentially weakly infected females, with 12, 9, 15, and 16 replicates, respectively. The insects presented a high negative geotaxis and a strong aggregation behavior whatever the sex or their infection. After an exploration phase, these behaviors were stable in time. The insects exhibited a preferential vertical position, head toward the top of the setup. Males had a higher negative geotaxis and a higher aggregation level than females. Both behaviors were enhanced in groups of 100% infected insects, the difference between sexes being maintained. According to a comparison between experimental and theoretical results, geotaxis favors the aggregation that mainly results from the inter-attraction between individuals.

A spatiotemporal analysis of the food dissemination process and the trophallactic network in the ant Lasius niger.

Intranidal food dissemination through trophallactic exchanges is a fundamental issue in social insect colonies but its underlying mechanisms are far from being clear. In light of the division of work, network theory and collective food management we develop a framework to investigate the spatiotemporal dynamics of the trophallactic network in starved Lasius niger ant colonies. Thanks to tracking methods we are able to record spatial locations of the trophallactic interactions in the nest. We highlight quantitative differences between the foragers and non-foragers concerning their contributions, their roles (donor/recipient) and their spatial distributions. Moreover, at the intracaste level, we show interindividual differences in all activities and we characterise their nature. In particular, within each caste, all the individuals have the same probability to start their food exchange activity but their probability to exchange differs after their first trophallactic event. Interestingly, despite the highlighted interindividual differences, the trophallactic network does not differ from a random network.

Division of labour in the black garden ant (Lasius niger) leads to three distinct proteomes.

Task specialization in social insects leads to striking intra-specific differences in behaviour, morphology, physiology and longevity, but the underlying mechanisms remain not yet fully understood. Adult colonies of black garden ants (Lasius niger) have a single queen fertilized by one or a small number of males. The inter-individual genetic variability is thus relatively low, making it easier to focus on the individual molecular differences linked to the division of labour. Mass spectrometry-based proteomics enabled us to highlight which biological functions create the difference between queens, foragers and nest-workers. The proteome of each caste reflected nicely their social role: e.g., reproduction for queens, pesticide resistance for foragers - that are the most exposed to environmental risk factors - and, interestingly, digestion for nest-workers, thus highlighting proteomic profiles differences even among workers. Furthermore, our exploratory approach suggests energy trade-off mechanisms - in connection with the theory of social immunity - that might explain the difference in longevity between queens and workers. This study brings evidence that proteomics is able to highlight the subtle mechanisms of molecular regulation induced by social organization.

Weber's Law-based perception and the stability of animal groups.

Group living animals form aggregations and flocks that remain cohesive in spite of internal movements of individuals. This is possible because individual group members repeatedly adjust their position and motion in response to the position and motion of other group members. Here, we develop a theoretical approach to address the question, what general features-if any-underlie the interaction rules that mediate group stability in animals of all species? We do so by considering how the spatial organization of a group would change in the complete absence of interactions. Without interactions, a group would disperse in a way that can be easily characterized in terms of Fick's diffusion equations. We can hence address the inverse theoretical problem of finding the individual-level interaction responses that are required to counterbalance diffusion and to preserve group stability. We show that an individual-level response to neighbour densities in the form of Weber's Law (a 'universal' law describing the functioning of the sensory systems of animals of all species) results in an 'anti-diffusion' term at the group level. On short timescales, this anti-diffusion restores the initial group configuration in a way that is reminiscent of methods for image deblurring in image processing. We also show that any non-homogeneous, spatial density distribution can be preserved over time if individual movement patterns have the form of a Weber's Law response. Weber's Law describes the fundamental functioning of perceptual systems. Our study indicates that it is also a necessary-but not sufficient-feature of collective interactions in stable animal groups.

Mixed-species aggregations in arthropods.

This review offers the first synthesis of the research on mixed-species groupings of arthropods and highlights the behavioral and evolutionary questions raised by such behavior. Mixed-species groups are commonly found in mammals and birds. Such groups are also observed in a large range of arthropod taxa independent of their level of sociality. Several examples are presented to highlight the mechanisms underlying such groupings, particularly the evidence for phylogenetic proximity between members that promotes cross-species recognition. The advantages offered by such aggregates are described and discussed. These advantages can be attributed to the increase in group size and could be identical to those of nonmixed groupings, but competition-cooperation dynamics might also be involved, and such effects may differ between homo- and heterospecific groups. We discuss three extreme cases of interspecific recognition that are likely involved in mixed-species groups as vectors for cross-species aggregation: tolerance behavior between two social species, one-way mechanism in which one species is attractive to others and two-way mechanism of mutual attraction. As shown in this review, the study of mixed-species groups offers biologists an interesting way to explore the frontiers of cooperation-competition, including the process of sympatric speciation.

Conflictual influence of humidity during shelter selection of the American cockroach (Periplaneta americana).

In collective decision-making, when confronted with different options, groups usually show a more marked preference for one of the options than do isolated individuals. This results from the amplification of individual preferences by social interactions within the group. We show, in an unusual counter-example, that when facing a binary choice between shelters with different relative humidities, isolated cockroaches of the species Periplaneta americana select the wettest shelter, while groups select the driest one. This inversion of selection results from a conflictual influence of humidity on the probabilities of entering and leaving each shelter. It is shown that the individual probability of entering the wettest shelter is higher than the group probability and is increased by previous entries and exits. The probability of leaving each shelter decreases in the population due to social interactions, but this decrease is less pronounced in the wettest shelter, suggesting weaker social interactions. A theoretical model is developed and highlights the existence of tipping points dependent on population size, beyond which an inversion of selection of a resting place is observed.

The role of personality variation, plasticity and social facilitation in cockroach aggregation.

Personality variation has been proven to affect ecology, evolution and group behaviour in many ways. Nevertheless, how social context influences behavioural strategies and individual personality variation has rarely been addressed. This study sheds light on the relationship between social interactions, personality variation and plasticity in a collective context. For this purpose, we used a binary setup (i.e. an arena with two identical shelters) to study the aggregation process of cockroaches. We tested the same individuals in isolated and social (groups of 16 individuals) conditions. We show that even if social interactions reduce the observation of personality variation, the behaviour in a group is correlated to individual preferences displayed in isolation. Furthermore, our results suggest that individuals show different levels of plasticity according to their shelter occupancy; individuals with high occupancy rates show low levels of plasticity and are less affected by social amplification in social conditions.