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.

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).

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.

The influence of the few: a stable 'oligarchy' controls information flow in house-hunting ants.

Animals that live together in groups often face difficult choices, such as which food resource to exploit, or which direction to flee in response to a predator. When there are costs associated with deadlock or group fragmentation, it is essential that the group achieves a consensus decision. Here, we study consensus formation in emigrating ant colonies faced with a binary choice between two identical nest-sites. By individually tagging each ant with a unique radio-frequency identification microchip, and then recording all ant-to-ant 'tandem runs'-stereotyped physical interactions that communicate information about potential nest-sites-we assembled the networks that trace the spread of consensus throughout the colony. Through repeated emigrations, we show that both the order in which these networks are assembled and the position of each individual within them are consistent from emigration to emigration. We demonstrate that the formation of the consensus is delegated to an influential but exclusive minority of highly active individuals-an 'oligarchy'-which is further divided into two subgroups, each specialized upon a different tandem running role. Finally, we show that communication primarily occurs between subgroups not within them, and further, that such between-group communication is more efficient than within-group communication.

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.

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.

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.

How collective comparisons emerge without individual comparisons of the options.

Collective decisions in animal groups emerge from the actions of individuals who are unlikely to have global information. Comparative assessment of options can be valuable in decision-making. Ant colonies are excellent collective decision-makers, for example when selecting a new nest-site. Here, we test the dependency of this cooperative process on comparisons conducted by individual ants. We presented ant colonies with a choice between new nests: one good and one poor. Using individually radio-tagged ants and an automated system of doors, we manipulated individual-level access to information: ants visiting the good nest were barred from visiting the poor one and vice versa. Thus, no ant could individually compare the available options. Despite this, colonies still emigrated quickly and accurately when comparisons were prevented. Individual-level rules facilitated this behavioural robustness: ants allowed to experience only the poor nest subsequently searched more. Intriguingly, some ants appeared particularly discriminating across emigrations under both treatments, suggesting they had stable, high nest acceptance thresholds. Overall, our results show how a colony of ants, as a cognitive entity, can compare two options that are not both accessible by any individual ant. Our findings illustrate a collective decision process that is robust to differences in individual access to information.

Landmarks and ant search strategies after interrupted tandem runs.

During a tandem run, a single leading ant recruits a single follower to an important resource such as a new nest. To examine this process, we used a motorized gantry, which has not previously been used in ant studies, to track tandem running ants accurately in a large arena and we compared their performance in the presence of different types of landmark. We interrupted tandem runs by taking away the leader and moved a large distant landmark behind the new nest just at the time of this separation. Our aim was to determine what information followers might have obtained from the incomplete tandem run they had followed, and how they behaved after the tandem run had been interrupted. Our results show that former followers search by using composite random strategies with elements of sub-diffusive and diffusive movements. Furthermore, when we provided more landmarks former followers searched for longer. However, when all landmarks were removed completely from the arena, the ants' search duration lasted up to four times longer. Hence, their search strategy changes in the presence or absence of landmarks. Even after extensive search of this kind, former followers headed back to their old nest but did not return along the path of the tandem run they had followed. The combination of the position to which the large distant landmark behind the new nest was moved and the presence or absence of additional landmarks influenced the orientation of the former followers' paths back to the old nest. We also found that these ants exhibit behavioural lateralization in which they possibly use their right eye more than their left eye to recognize landmarks for navigation. Our results suggest that former follower ants learn landmarks during tandem running and use this information to make strategic decisions.

Ants show a leftward turning bias when exploring unknown nest sites.

Behavioural lateralization in invertebrates is an important field of study because it may provide insights into the early origins of lateralization seen in a diversity of organisms. Here, we present evidence for a leftward turning bias in Temnothorax albipennis ants exploring nest cavities and in branching mazes, where the bias is initially obscured by thigmotaxis (wall-following) behaviour. Forward travel with a consistent turning bias in either direction is an effective nest exploration method, and a simple decision-making heuristic to employ when faced with multiple directional choices. Replication of the same bias at the colony level would also reduce individual predation risk through aggregation effects, and may lead to a faster attainment of a quorum threshold for nest migration. We suggest the turning bias may be the result of an evolutionary interplay between vision, exploration and migration factors, promoted by the ants' eusociality.

Trail laying during tandem-running recruitment in the ant Temnothorax albipennis.

Tandem running is a recruitment strategy whereby one ant leads a single naïve nest mate to a resource. While tandem running progresses towards the goal, the leader ant and the follower ant maintain contact mainly by tactile signals. In this paper, we investigated whether they also deposit chemical signals on the ground during tandem running. We filmed tandem-running ants and analysed the position of the gasters of leaders and followers. Our results show that leader ants are more likely to press their gasters down to the substrate compared to follower ants, single ants and transporter ants. Forward tandem-run leaders (those moving towards a new nest site) performed such trail-marking procedures three times more often than reverse tandem leaders (those moving towards an old nest site). That leader ants marked the trails more often during forward tandem runs may suggest that it is more important to maintain the bond with the follower ant on forward tandem runs than on reverse tandem runs. Marked trails on the ground may serve as a safety line that improves both the efficiency of tandem runs and their completion rates.

Seeking safety: Movement dynamics after post-contact immobility.

Post-contact immobility (PCI) is a final attempt to avoid predation. Here, for the first time, we examine the pattern of movement and immobility when antlion larvae resume activity after PCI. To simulate contact with, and escape from, a predator we dropped the larvae onto three different substrates: Paper, Shallow sand (2.3mm-deep) and Deep sand (4.6mm-deep). The Paper lining a Petri dish represented a hard surface that antlion larvae could not penetrate to hide. The Shallow sand permitted the antlions to dig but not to submerge completely whereas the Deep sand allowed them both to dig and to submerge. We tracked their paths automatically and recorded alternating immobility and movement durations over 90min. On the impenetrable substrate, antlion larvae showed super-diffusive dispersal, their movement durations became longer, their immobility durations became shorter and their instantaneous speeds increased. This is consistent with the antlions needing to leave an area of hard substrate and quickly to find somewhere to hide. On Shallow sand, antlion larvae exhibited a modest increase in movement duration, a modest decrease in immobility duration and a concomitant diffusive dispersal. This is consistent with their use of a spiral search, presumably for a suitable depth of sand, to conceal themselves. On Deep sand, the movement and immobility durations of the antlion larvae did not change and their dispersal was sub-diffusive because they were able to bury themselves. On Paper, the distribution of immobility durations had a long tail, consistent with a log-normal distribution. On Shallow and Deep sand, most of the distribution was fitted better by a power law or a log-normal. Our results suggest that PCI in antlion larvae is a disruptive event and that post-PCI movement and immobility gradually return to the pattern typical of intermittent locomotion, depending on the scope for burying and hiding in the substrate.

Economic investment by ant colonies in searches for better homes.

Organisms should invest more in gathering information when the pay-off from finding a profitable resource is likely to be greater. Here, we ask whether animal societies put more effort in scouting for a new nest when their current one is of low quality. We measured the scouting behaviour of Temnothorax albipennis ant colonies when they inhabit nest-sites with different combinations of desirable attributes. We show that the average probability of an ant scouting decreases significantly with an increase in the quality of the nest in which the colony currently resides. This means that the greater the potential gain from finding a new nest, the more effort a colony puts into gathering information regarding new nest-sites. Our results show, for the first time to our knowledge, the ability of animal societies to respond collectively to the quality of a resource they currently have at their disposal (e.g. current nest-site) and regulate appropriately their information gathering efforts for finding an alternative (e.g. a potentially better nest-site).

The interplay between scent trails and group-mass recruitment systems in ants.

Large ant colonies invariably use effective scent trails to guide copious ant numbers to food sources. The success of mass recruitment hinges on the involvement of many colony members to lay powerful trails. However, many ant colonies start off as single queens. How do these same colonies forage efficiently when small, thereby overcoming the hurdles to grow large? In this paper, we study the case of combined group and mass recruitment displayed by some ant species. Using mathematical models, we explore to what extent early group recruitment may aid deployment of scent trails, making such trails available at much smaller colony sizes. We show that a competition between group and mass recruitment may cause oscillatory behaviour mediated by scent trails. This results in a further reduction of colony size to establish trails successfully.

Experience, corpulence and decision making in ant foraging.

Social groups are structured by the decisions of their members. Social insects typically divide labour: some decide to stay in the nest while others forage for the colony. Two sources of information individuals may use when deciding whether to forage are their own experience of recent task performance and their own physiology, e.g. fat reserves (corpulence). The former is primarily personal information; the latter may give an indication of the food reserves of the whole colony. These factors are hard to separate because typically leaner individuals are also more experienced foragers. We designed an experiment to determine whether foraging specialisation is physiological or experience based (or both). We invented a system of automatic doors controlled by radio-tag information to manipulate task access and decouple these two sources of information. Our results show that when information from corpulence and recent experience conflict, ants behave only in accordance with their corpulence. However, among ants physiologically inclined to forage (less corpulent ants), recent experience of success positively influenced their propensity to forage again. Hence, foraging is organised via long-term physiological differences among individuals resulting in a relatively stable response threshold distribution, with fine-tuning provided by short-term learning processes. Through these simple rules, colonies can organise their foraging effort both robustly and flexibly.

Do ants need to be old and experienced to teach?

Learning is widespread in invertebrates. However, whether social insects improve their recruitment skills with experience is only beginning to be investigated. Tandem running is a one-to-one form of recruitment used by certain species of ant. It is a remarkable communication system that meets widely accepted criteria for teaching in non-human animals. Here, we determined experimentally to what extent participation in, and efficient execution of, tandem running depends on either the age or the experience of worker ants. To investigate these issues, we constructed colonies of the ant Temnothorax albipennis with different compositions of inexperienced and experienced workers from different age cohorts and then examined which ants participated in tandem runs when they emigrated. Our results show that the ability to participate actively in recruitment by tandem running is present in all worker age groups but the propensity to participate varies with experience rather than age per se. Experienced individuals were more likely to engage in tandem runs, either as leaders or as followers, than young inexperienced individuals, and older experienced ants were more likely to lead tandems than older inexperienced ants. Young inexperienced ants led faster, more rapidly dispersing and less accurately orientated tandem runs than the older experienced ants. Our study suggests that experience (rather than age per se) coupled to stimulus threshold responses might interact to promote a division of labour so that a suitable number of workers actively participate in tandem runs.

Teaching in tandem-running ants.

The ant Temnothorax albipennis uses a technique known as tandem running to lead another ant from the nest to food--with signals between the two ants controlling both the speed and course of the run. Here we analyse the results of this communication and show that tandem running is an example of teaching, to our knowledge the first in a non-human animal, that involves bidirectional feedback between teacher and pupil. This behaviour indicates that it could be the value of information, rather than the constraint of brain size, that has influenced the evolution of teaching.

Knowledgeable individuals lead collective decisions in ants.

Self-organisation underlies many collective processes in large animal groups, where coordinated patterns and activities emerge at the group level from local interactions among its members. Although the importance of key individuals acting as effective leaders has recently been recognised in certain collective processes, it is widely believed that self-organised decisions are evenly shared among all or a subset of individuals acting as decision-makers, unless there are significant conflicts of interests among group members. Here, we show that certain individuals are disproportionately influential in self-organised decisions in a system where all individuals share the same interests: nest site selection by the ant Temnothorax albipennis. Workers that visited a good available nest site prior to emigration (the familiar nest) memorised its location, and later used this memory to navigate efficiently and find that nest faster than through random exploration. Additionally, these workers relied on their private information to expedite individual decisions about the familiar nest. This conferred a bias in favour of familiar nests over novel nests during emigrations. Informed workers were shown to have a significantly greater share in both recruitment and transport to the familiar nest than naïve workers. This suggests that they were the main determinants of the collective preference for familiar nests, and thus contributed greatly to enhance collective performance. Overall, these results indicate that self-organised decisions are not always evenly shared among decision-makers, even in systems where there are no conflicts of interest. Animal groups may instead benefit from well-informed, knowledgeable individuals acting as leaders in decisions.