Robotic communication with ants.

We used a robotic gantry to test the hypothesis that tandem running in the ant Temnothorax albipennis can be successful in the absence of trail laying by the leader. Pheromone glands were placed on a pin attached to a gantry. This set-up substituted for the leader of a tandem run. Neither the pin nor the glands touched the substrate and thus the ant following the robot was tracking a plume of airborne pheromones. The robot led individual workers from their current nest to a potential new one. The robotic gantry was programmed to allow for human intervention along its path to permit the following ant to stop and survey its surroundings and then catch up with its mechanical leader. The gantry then automatically tracked the precise route taken by each ant from the new nest back to the old one. Ants led by the robot were significantly more successful at finding their way home than those we carried to the new nest that had no opportunity to learn landmarks. The robot was programmed to take either a straight or a sinusoidal path to the new nest. However, we found no significant difference in the abilities of ants that had been led on such direct or sinuous paths to find their way home. Here, the robot laid no trail but our findings suggest that, under such circumstances, the following ant may lay a trail to substitute for the missing one.

Hide-and-seek strategies and post-contact immobility.

To understand why an animal might gain by playing dead, or more precisely, exhibit post-contact immobility (PCI), we consider the context in which this behaviour occurs. Is it, for example, a method by which a potential victim encourages a predator to direct its attention elsewhere? We investigate this possibility by using the marginal value theorem to analyse predator behaviour in the context of this defence strategy by potential prey. We consider two models. In the first, (random revisiting) the predator may return to sites it has already depleted within the patch. In the second, (systematic search) the predator goes only to new sites within the patch. The results of the two models are qualitatively extremely similar. We show that when prey occur in patches, PCI favours prey survival. Indeed, certain antlion larvae have PCI durations characterized by very long half-lives. These appear to be of such long durations that further increases would convey no substantial benefits in redirecting potential predators to other antlions within the patch and subsequently to other patches.

Reconstructing the Intrinsic Statistical Properties of Intermittent Locomotion Through Corrections for Boundary Effects.

Locomotion characteristics are often recorded within bounded spaces, a constraint which introduces geometry-specific biases and potentially complicates the inference of behavioural features from empirical observations. We describe how statistical properties of an uncorrelated random walk, namely the steady-state stopping location probability density and the empirical step probability density, are affected by enclosure in a bounded space. The random walk here is considered as a null model for an organism moving intermittently in such a space, that is, the points represent stopping locations and the step is the displacement between them. Closed-form expressions are derived for motion in one dimension and simple two-dimensional geometries, in addition to an implicit expression for arbitrary (convex) geometries. For the particular choice of no-go boundary conditions, we demonstrate that the empirical step distribution is related to the intrinsic step distribution, i.e. the one we would observe in unbounded space, via a multiplicative transformation dependent solely on the boundary geometry. This conclusion allows in practice for the compensation of boundary effects and the reconstruction of the intrinsic step distribution from empirical observations.

Animal intermittent locomotion: A null model for the probability of moving forward in bounded space.

We present a null model to be compared with biological data to test for intrinsic persistence in movement between stops during intermittent locomotion in bounded space with different geometries and boundary conditions. We describe spatio-temporal properties of the sequence of stopping points r1,r2,r3,… visited by a Random Walker within a bounded space. The path between stopping points is not considered, only the displacement. Since there are no intrinsic correlations in the displacements between stopping points, there is no intrinsic persistence in the movement between them. Hence, this represents a null-model against which to compare empirical data for directional persistence in the movement between stopping points when there is external bias due to the bounded space. This comparison is a necessary first step in testing hypotheses about the function of the stops that punctuate intermittent locomotion in diverse organisms. We investigate the probability of forward movement, defined as a deviation of less than 90° between two successive displacement vectors, as a function of the ratio between the largest displacement between stops that could be performed by the random walker and the system size, α=Δℓ/Lmax. As expected, the probability of forward movement is 1/2 when α→0. However, when α is finite, this probability is less than 1/2 with a minimum value when α=1. For certain boundary conditions, the minimum value is between 1/3 and 1/4 in 1D while it can be even lower in 2D. The probability of forward movement in 1D is calculated exactly for all values 0<α⩽1 for several boundary conditions. Analytical calculations for the probability of forward movement are performed in 2D for circular and square bounded regions with one boundary condition. Numerical results for all values 0<α⩽1 are presented for several boundary conditions. The cases of rectangle and ellipse are also considered and an approximate model of the dependence of the forward movement probability on the aspect ratio is provided. Finally, some practical points are presented on how these results can be utilised in the empirical analysis of animal movement in two-dimensional bounded space.

Post-contact immobility and half-lives that save lives.

A wide variety of animals become completely immobile after initial contact with a potential predator. This behaviour is considered to be a last-ditch escape strategy. Here, we test the hypothesis that such immobility should have an extremely unpredictable duration. We find that it spans more than three orders of magnitude in antlion larvae. We also analyse the second period of immobility that follows the first bout of immobility, and consider the distributions of both first and second immobility periods within the context of the intermittence that characterizes the movement of most organisms. Both immobility durations were fitted best by exponential distributions. Therefore, both were characterized by high variability and hence, unpredictability. The immobility half-life, its mean duration and standard deviation were greater for the first than the second immobility. Furthermore, individual consistency was weak or absent in repeated measures of the first immobility and between the first and second immobilities. Our quantitative approach can be replicated across taxa and would help link an understanding of immobility after an initial predator contact in both vertebrates and invertebrates. To facilitate this, we contend that the terminology should be simplified, and we advocate the use of the term post-contact immobility (PCI).

Social flocculation in plant-animal worms.

Individual animals can often move more safely or more efficiently as members of a group. This can be as simple as safety in numbers or as sophisticated as aerodynamic or hydrodynamic cooperation. Here, we show that individual plant-animal worms (Symsagittifera roscoffensis) can move to safety more quickly through flocculation. Flocs form in response to turbulence that might otherwise carry these beach-dwelling worms out to sea. They allow the worms to descend much more quickly to the safety of the substrate than single worms could swim. Descent speed increases with floc size such that larger flocs can catch up with smaller ones and engulf them to become even larger and faster. To our knowledge, this is the first demonstration of social flocculation in a wild, multicellular organism. It is also remarkable that such effective flocculation occurs where the components are comparatively large multicellular organisms organized as entangled ensembles.

Digging the optimum pit: antlions, spirals and spontaneous stratification.

Most animal traps are constructed from self-secreted silk, so antlions are rare among trap builders because they use only materials found in the environment. We show how antlions exploit the properties of the substrate to produce very effective structures in the minimum amount of time. Our modelling demonstrates how antlions: (i) exploit self-stratification in granular media differentially to expose deleterious large grains at the bottom of the construction trench where they can be ejected preferentially, and (ii) minimize completion time by spiral rather than central digging. Both phenomena are confirmed by our experiments. Spiral digging saves time because it enables the antlion to eject material initially from the periphery of the pit where it is less likely to topple back into the centre. As a result, antlions can produce their pits-lined almost exclusively with small slippery grains to maximize powerful avalanches and hence prey capture-much more quickly than if they simply dig at the pit's centre. Our demonstration, for the first time to our knowledge, of an animal using self-stratification in granular media exemplifies the sophistication of extended phenotypes even if they are only formed from material found in the animal's environment.

Plant-animal worms round themselves up in circular mills on the beach.

Collective motion is a fascinating and intensely studied manifestation of collective behaviour. Circular milling is an impressive example. It occurs in fishes, processionary caterpillars and army ants, among others. Its adaptive significance, however, is not yet well understood. Recently, we demonstrated experimentally circular milling in the marine plant-animal worm Symsagittifera roscoffensis. We hypothesized that its function is to gather the worms and facilitate the dense films they form on the beach to promote the photosynthesis of their symbiotic algae. Here, we report for the first time, to our knowledge, the occurrence of S. roscoffensis circular mills in nature and show that it is by no means rare. The size and behaviour of circular mills in their natural environment is compatible with our earlier experimental results. This makes S. roscoffensis a good study system for understanding the proximate and ultimate mechanisms of circular milling.

Asymmetric ommatidia count and behavioural lateralization in the ant Temnothorax albipennis.

Workers of the house-hunting ant Temnothorax albipennis rely on visual edge following and landmark recognition to navigate their rocky environment, and they also exhibit a leftward turning bias when exploring unknown nest sites. We used electron microscopy to count the number of ommatidia composing the compound eyes of workers, males and queens, to make an approximate assessment of their relative sampling resolution; and to establish whether there is an asymmetry in the number of ommatidia composing the workers' eyes, which might provide an observable, mechanistic explanation for the turning bias. We hypothesise that even small asymmetries in relative visual acuity between left and right eyes could be magnified by developmental experience into a symmetry-breaking turning preference that results in the inferior eye pointing toward the wall. Fifty-six workers were examined: 45% had more ommatidia in the right eye, 36% more in the left, and 20% an equal number. A tentative connection between relative ommatidia count for each eye and turning behaviour was identified, with a stronger assessment of behavioural lateralization before imaging and a larger sample suggested for further work. There was a clear sexual dimorphism in ommatidia counts between queens and males.

Complementary landmarks facilitate ant navigation.

Visual landmarks are important navigational aids to many animals, and when more than one is available their juxtaposition can convey valuable new information to a navigator about progress toward a goal, depending on the landmarks' comparative distinctiveness. We investigated the effect of presenting rock ant colonies (Temnothorax albipennis) with identical horizontal landmarks either side of their route, versus one horizontal landmark paired with a sloping landmark, as they navigated to a new nest site. Our findings suggest that ants can obtain more navigational information from a combination of dissimilar landmarks: the average tortuosity of the route taken between old and new nests was significantly lower when a horizontal landmark was paired with a monotonically downward sloping landmark (the paths were more direct). The impact on available navigational information from the similarity or dissimilarity of nearby landmarks is likely made through more distinctive visual panoramas, and could be an influential factor in individual and collective animal decision-making about which routes are followed. Furthermore, the effect of landmark complementarity may be relevant to a wide range of species, including other insects or birds, and highlights the possibility that there is an intrinsic difference in the informational content of natural vs. artificial environments.

Measuring site fidelity and spatial segregation within animal societies.

Animals often display a marked tendency to return to previously visited locations that contain important resources, such as water, food, or developing brood that must be provisioned. A considerable body of work has demonstrated that this tendency is strongly expressed in ants, which exhibit fidelity to particular sites both inside and outside the nest. However, thus far many studies of this phenomena have taken the approach of reducing an animal's trajectory to a summary statistic, such as the area it covers.Using both simulations of biased random walks, and empirical trajectories from individual rock ants, Temnothorax albipennis, we demonstrate that this reductive approach suffers from an unacceptably high rate of false negatives.To overcome this, we describe a site-centric approach which, in combination with a spatially-explicit null model, allows the identification of the important sites towards which individuals exhibit statistically significant biases.Using the ant trajectories, we illustrate how the site-centric approach can be combined with social network analysis tools to detect groups of individuals whose members display similar space-use patterns.We also address the mechanistic origin of individual site fidelity; by examining the sequence of visits to each site, we detect a statistical signature associated with a self-attracting walk - a non-Markovian movement model that has been suggested as a possible mechanism for generating individual site fidelity.

Variability in individual assessment behaviour and its implications for collective decision-making.

Self-organized systems of collective behaviour have been demonstrated in a number of group-living organisms. There is, however, less research relating to how variation in individual assessments may facilitate group decision-making. Here, we investigate this using the decentralized system of collective nest choice behaviour employed by the ant Temnothorax albipennis, combining experimental results with computational modelling. In experiments, isolated workers of this species were allowed to investigate new nest sites of differing quality, and it was found that for any given nest quality, there was wide variation among individuals in the durations that they spent within each nest site. Additionally, individual workers were consistent in spending more time in nest sites of higher quality, and less time in those of lower quality. Hence, the time spent in a new nest site must have included an assessment of nest quality. As nest site visit durations (henceforth termed assessment durations) are linked to recruitment, it is possible that the variability we observed may influence the collective decision-making process of colonies. Thus, we explored this further using a computational model of nest site selection, and found that heterogeneous nest assessments conferred a number of potential benefits. Furthermore, our experiments showed that nest quality assessments were flexible, being influenced by experience of prior options. Our findings help to elucidate the potential mechanisms underlying group behaviour, and highlight the importance of heterogeneity among individuals, rather than precise calibration, in shaping collective decision-making.

A social mechanism facilitates ant colony emigrations over different distances.

Behavioural responses enable animals to react rapidly to fluctuating environments. In eusocial organisms, such changes are often enacted at the group level, but may be organised in a decentralised fashion by the actions of individuals. However, the contributions of different group members are rarely homogeneous, and there is evidence to suggest that certain 'keystone' individuals are important in shaping collective responses. Accordingly, investigations of the dynamics and structuring of behavioural changes at both the group and individual level are crucial for evaluating the relative influence of different individuals. Here, we examined the composition of tandem running behaviour during colony emigrations in the ant species Temnothorax albipennis Tandem running is modulated in response to emigration distance, with more runs being conducted when a more distant nest site must be reached. We show that certain individuals are highly active in the tandem running process, attempting significantly more work in the task. Contrary to expectations, however, such individuals are in fact no more successful at conducting tandem runs than their less active nest mates. Instead, it seems that when more tandem runs are required, colonies rely on greater recruitment of workers into the process. The implications of our study are that in some cases, even when apparently 'key' individuals exist within a group, their relative contribution to task performance may be far from decisive.

Migration control: a distance compensation strategy in ants.

Migratory behaviour forms an intrinsic part of the life histories of many organisms but is often a high-risk process. Consequently, varied strategies have evolved to negate such risks, but empirical data relating to their functioning are limited. In this study, we use the model system of the house-hunting ant Temnothorax albipennis to demonstrate a key strategy that can shorten migration exposure times in a group of social insects. Colonies of these ants frequently migrate to new nest sites, and due to the nature of their habitat, the distances over which they do so are variable, leading to fluctuating potential costs dependent on migration parameters. We show that colonies of this species facultatively alter the dynamics of a migration and so compensate for the distance over which a given migration occurs. Specifically, they achieve this by modulating the rate of 'tandem running', in which workers teach each other the route to a new nest site. Using this method, colonies are able to engage a larger number of individuals in the migration process when the distance to be traversed is greater, and furthermore, the system appears to be based on perceived encounter rate at the individual level. This form of decentralised control highlights the adaptive nature of a behaviour of ecological importance, and indicates that the key to its robustness lies in the use of simple rules. Additionally, our results suggest that such coordinated group reactions are central to achieving the high levels of ecological success seen in many eusocial organisms.

Social behaviour and collective motion in plant-animal worms.

Social behaviour may enable organisms to occupy ecological niches that would otherwise be unavailable to them. Here, we test this major evolutionary principle by demonstrating self-organizing social behaviour in the plant-animal, Symsagittifera roscoffensis. These marine aceol flat worms rely for all of their nutrition on the algae within their bodies: hence their common name. We show that individual worms interact with one another to coordinate their movements so that even at low densities they begin to swim in small polarized groups and at increasing densities such flotillas turn into circular mills. We use computer simulations to: (i) determine if real worms interact socially by comparing them with virtual worms that do not interact and (ii) show that the social phase transitions of the real worms can occur based only on local interactions between and among them. We hypothesize that such social behaviour helps the worms to form the dense biofilms or mats observed on certain sun-exposed sandy beaches in the upper intertidal of the East Atlantic and to become in effect a super-organismic seaweed in a habitat where macro-algal seaweeds cannot anchor themselves. Symsagittifera roscoffensis, a model organism in many other areas in biology (including stem cell regeneration), also seems to be an ideal model for understanding how individual behaviours can lead, through collective movement, to social assemblages.

Exploration adjustment by ant colonies.

How do animals in groups organize their work? Division of labour, i.e. the process by which individuals within a group choose which tasks to perform, has been extensively studied in social insects. Variability among individuals within a colony seems to underpin both the decision over which tasks to perform and the amount of effort to invest in a task. Studies have focused mainly on discrete tasks, i.e. tasks with a recognizable end. Here, we study the distribution of effort in nest seeking, in the absence of new nest sites. Hence, this task is open-ended and individuals have to decide when to stop searching, even though the task has not been completed. We show that collective search effort declines when colonies inhabit better homes, as a consequence of a reduction in the number of bouts (exploratory events). Furthermore, we show an increase in bout exploration time and a decrease in bout instantaneous speed for colonies inhabiting better homes. The effect of treatment on bout effort is very small; however, we suggest that the organization of work performed within nest searching is achieved both by a process of self-selection of the most hard-working ants and individual effort adjustment.

Ants determine their next move at rest: motor planning and causality in complex systems.

To find useful work to do for their colony, individual eusocial animals have to move, somehow staying attentive to relevant social information. Recent research on individual Temnothorax albipennis ants moving inside their colony's nest found a power-law relationship between a movement's duration and its average speed; and a universal speed profile for movements showing that they mostly fluctuate around a constant average speed. From this predictability it was inferred that movement durations are somehow determined before the movement itself. Here, we find similar results in lone T. albipennis ants exploring a large arena outside the nest, both when the arena is clean and when it contains chemical information left by previous nest-mates. This implies that these movement characteristics originate from the same individual neural and/or physiological mechanism(s), operating without immediate regard to social influences. However, the presence of pheromones and/or other cues was found to affect the inter-event speed correlations. Hence we suggest that ants' motor planning results in intermittent response to the social environment: movement duration is adjusted in response to social information only between movements, not during them. This environmentally flexible, intermittently responsive movement behaviour points towards a spatially allocated division of labour in this species. It also prompts more general questions on collective animal movement and the role of intermittent causation from higher to lower organizational levels in the stability of complex systems.

Differentiated Anti-Predation Responses in a Superorganism.

Insect societies are complex systems, displaying emergent properties much greater than the sum of their individual parts. As such, the concept of these societies as single 'superorganisms' is widely applied to describe their organisation and biology. Here, we test the applicability of this concept to the response of social insect colonies to predation during a vulnerable period of their life history. We used the model system of house-hunting behaviour in the ant Temnothorax albipennis. We show that removing individuals from directly within the nest causes an evacuation response, while removing ants at the periphery of scouting activity causes the colony to withdraw back into the nest. This suggests that colonies react differentially, but in a coordinated fashion, to these differing types of predation. Our findings lend support to the superorganism concept, as the whole society reacts much like a single organism would in response to attacks on different parts of its body. The implication of this is that a collective reaction to the location of worker loss within insect colonies is key to avoiding further harm, much in the same way that the nervous systems of individuals facilitate the avoidance of localised damage.

How ants use quorum sensing to estimate the average quality of a fluctuating resource.

We show that one of the advantages of quorum-based decision-making is an ability to estimate the average value of a resource that fluctuates in quality. By using a quorum threshold, namely the number of ants within a new nest site, to determine their choice, the ants are in effect voting with their feet. Our results show that such quorum sensing is compatible with homogenization theory such that the average value of a new nest site is determined by ants accumulating within it when the nest site is of high quality and leaving when it is poor. Hence, the ants can estimate a surprisingly accurate running average quality of a complex resource through the use of extraordinarily simple procedures.

Universality in ant behaviour.

Prediction for social systems is a major challenge. Universality at the social level has inspired a unified theory for urban living but individual variation makes predicting relationships within societies difficult. Here, we show that in ant societies individual average speed is higher when event duration is longer. Expressed as a single scaling function, this relationship is universal because for any event duration an ant, on average, moves at the corresponding average speed except for a short acceleration and deceleration at the beginning and end. This establishes cause and effect within a social system and may inform engineering and control of artificial ones.