Insect. Soc. (2014) 61:1–8 DOI 10.1007/s00040-013-0325-3 Insectes Sociaux

REVIEW ARTICLE

The journey of tandem running: the twists, turns and what we have learned

E. L. Franklin

Received: 4 February 2013 / Revised: 28 October 2013 / Accepted: 4 November 2013 / Published online: 21 November 2013 Ó International Union for the Study of Social (IUSSI) 2013

Abstract Tandem running, whereby one worker recruits acquired slave workers back to the slaver’s home nest another is utilised by many . Since first being (Buschinger et al., 1980). recorded, it has provided a valuable experimental tool for Wilson (1959) described tandem running, in the ant testing hypotheses about collective decision making, com- Cardiocondyla, as a communication method used munication and even teaching. In this review I explore the by workers to recruit others to food sources. This method journey tandem running has taken, the twists and turns in the of communication differed from the pheromone mass theories surrounding it and what tandem running has taught recruitment, trail laying behaviour used by worker to us. This review examines the empirical research conducted recruit other workers (Wilson, 1971). Foraging trails are on tandem running, from when it was first described, con- created when on finding a food source, a worker leaves a siders the theories that have arisen from that research and pheromone trail from it back to the nest. The trail stim- ultimately what has been learnt and what is still yet to be ulates other workers to follow the trail to the food source. explored. These workers, who have followed the trail, return to the nest reinforcing the trail with their own pheromones. Keywords Tandem running Á Collective decision making Á Thus, increasing the number of foragers recruited to the Social learning Á Teaching food source by positive feedback (Wilson, 1971; Sumpter and Brannstrom, 2008). In contrast, tandem running workers, appeared not to deposit pheromone trails (Wil- Introduction son, 1959). Instead, a curious interaction between a leader (an ant with knowledge of the location of a food source) Tandem running was first recorded as early as 1896 (Ald- and a naive follower occurred. The leader emerged from lerz, 1896 as cited in Stuart, 1986; Hingston, 1929) and has the nest with the follower close behind. The leader then since been described in a diverse array of ant species within ran forward a few body lengths and then stopped, the subfamilies , Formicinae, and Ponerinae awaiting antennation from the follower on her legs or (for a full list of genera and species with identified tandem gaster. With contact from the follower, the leader pro- running see Table 1). This review focuses on instances of gressed again (Fig. 1). This interaction between leader tandem running where it is used within ant colonies to and follower continued until the pair reached the food recruit to food or new nest sites. However, tandem running source. Although tandem running workers do not use is also used by some ant species to recruit nestmates to raid mass recruitment pheromone trails during recruitment, other ant colonies for slaves and even to recruit newly pheromones appear important for tandem run initiation (tandem calling) and pair cohesion (Ho¨lldobler et al., 1974;Mo¨glich et al., 1974;Ho¨lldobler and Traniello, E. L. Franklin (&) 1980). The use of pheromones in tandem running has been School of Applied Sciences, Bournemouth University, demonstrated experimentally, showing that a following worker Christchurch House, Talbot Campus, Fern Barrow, Poole, Dorset BH12 5BB, UK of a tandem pair can be led using a glass bead, providing it e-mail: [email protected] possesses pheromones similar to those of its previous leader 123 2 E. L. Franklin

Table 1 A table of all the identified instances and contexts of tandem running throughout the Myrmicinae, Formacinae and Ponerinae sub- families of ants Subfamily Species or Genera Tandem Reference running recruitment context

Myrmicinae Cardiocondyla Food Wilson 1959 venustula Myrmicinae Cardiocondyla Food Wheeler 1908 cited emeryi in Wilson 1959 Formicinae Camponotus Food and Ho¨lldobler et al. sericeus nest 1974 Formicinae Camponotus Food and Ho¨lldobler 1971 socius nest Myrmicinae Food Lane 1977 unifasciatus (Previously Leptothorax) Myrmicinae Leptothorax Food and Mo¨glich et al. 1974 acervorum nest Temnothorax nylanderi (Previously Leptothorax) Leptothorax muscorum Leptothorax crassipilis Myrmicinae Harpagoxenus Slave raids Buschinger et al. canadensis 1980 Chalepoxenus muellerianus Myrmicinae Harpagoxenus Slave raids Buschinger and sublaevis Winter 1977 Myrmicinae Temnothorax Food and Mallon et al. 2001, Fig. 1 A diagram of a tandem run showing how the leader interacts albipennis nest Franks and with her follower. This image was drawn by E. Franklin from a video Richardson 2006 of Temnothorax albipennis performing a tandem run. The video was Myrmicinae Tomognathus Nest Adlerz 1986 also recorded by E. Franklin sublaevis Formicinae Polyrhachis Food Liefke et al. 2001 proxima Communication by tandem running has been deemed Ponerinae Mesoponera Food Agbogba 1984 primitive by some, since it lacked the mass recruitment of caffraria trail following (Hingston, 1929). Consequently, tandem Hypoponera sp. running was described as an evolutionary precursor to trail Ponerinae Pachycondyla Food and Jessen and following (Hingston, 1929). However, more recently it has tesserinoda nest Maschwitz 1986, been shown that the species that use tandem running have (previously Maschwitz et al. small to medium sized colonies, that would not have a large Bothroponera) 1974 enough number of foraging workers to perform pheromone Ponerinae Pachycondyla Nest Fresneau 1985 trail recruitment (Beckers et al., 1989; Mailleux et al., 2003; apicalis Planque´, 2010). Therefore, tandem running is likely to be an Ponerinae Pachycondyla Food Fresneau 1985 villosa evolved strategy used by small colonies rather than being a primitive strategy. Mo¨glich (1978) found that tandem running ant species, (Ho¨lldobler et al., 1974;Mo¨glich et al., 1974). However, with small colony sizes, living in fragile nests, for example there has been little or no exploration into tandem run the genera Temnothorax, formally Leptothorax, not only pheromones since these early studies. used to tandem running recruit others to food but was also

123 The journey of tandem running: the twists, turns and what we have learned 3 used in colony emigration to new nest sites (Mo¨glich, 1978). are used by colonies in emigrations especially when there Mo¨glich showed that workers recruited others to new nest have been few forward tandem runs. This may occur sites by tandem running and followers of these tandem runs because there were limited numbers of potential followers at could become active in the emigration and start recruiting the old nest (Pratt et al., 2002) or the new nest was easy to further workers (Mo¨glich, 1978). He also described the find without the need for forward tandem runs (Langridge sequence of events these ants go through to emigrate to a et al., 2004) and the workers switched to carrying due to the new nest. Initially, scouts leave the old nest to search for quorum number met rapidly. In these situations, reverse new sites, on finding a site they recruit to it by tandem tandem runs can increase the number of active recruiters to running, ‘recruiting recruiters’. Second, the colony switches move the colony. This allows colonies to speed up emi- to carrying the remaining colony members (workers, brood grations that may have started slowly due to there being few and queen) to the new nest (Mo¨glich, 1978). Experimental active scouts in the forward tandem running recruitment manipulation of the sequence of events in an emigration phase (Pratt et al., 2002). However, the information we became fundamental in the later studies of decentralised possess about reverse tandem runs is limited to these few collective decision making in ants. studies and the remainder of this review focuses on forward tandem runs, unless stated otherwise. Ant colonies can also use a decision making process to Collective decision making decide between multiple choices of nest, with varying quality and consistently choose the best option. Mallon and There have been a number of studies that have used nest Franks (2000) were the first to explore the ant colonies emigrations, in Temnothorax sp., to ask questions about complex decision making with most of the scouting ants collective decision making (Mallon and Franks, 2000; only visiting one of the options (Mallon and Franks, 2000). Mallon et al., 2001; Pratt et al., 2002; Pratt, 2008). These Somehow, the ant colonies could choose the better of two studies linked the individual actions of scouts to the col- options with limited direct comparisons. It was suggested lective decision making of an . These studies, that potential new nest sites competed for committed amongst others, gave us a greater understanding of the workers, to recruit to them and that it was the quality of the emigration process. This process is as follows; if the nest, a nest that dictated how quickly workers started recruiting to colony of Temnothorax ants currently inhabit is damaged or them (recruitment latency). Positive feedback of workers destroyed, scouts will leave the nest in search of a suitable recruiting more rapidly to higher quality nests would lead to new nest site. On a scout finding a potential nest she assesses the quorum number being met first in the most desirable nest its quality (Mallon and Franks, 2000; Franks et al., 2003; and therefore being the one into which the colony moves Franks et al., 2006). If it is suitable by her standards she (Mallon et al., 2001). But what happens if the high quality returns to the nest and recruits others to this new potential nest is a long way away? Surely, any latency differences nest site by tandem running. If the recruited worker assesses would be negated and the colonies could no longer choose the nest to have high enough quality to recruit to they can go between options due to the time it would take to travel to far, on to be the leaders of subsequent tandem runs to the new high quality nest? Franks et al. (2008) explored this question nest site. This recruitment continues until a number of and discovered that colonies of ants could indeed choose the workers are present in the new nest site at which point the better nest, even if it was nine times further away than the workers will switch to carrying the remaining colony poor one (Franks et al., 2008). They then suggested that members (which is much quicker). The number of indi- recruitment latency alone could not be the key to a colony’s viduals in the new nest site, at the point at which the ants decision making, as the colony could still make the correct switch to carrying, is referred to as the quorum number decision despite any differences in recruitment latency. (Pratt et al., 2002; Pratt, 2008). In addition to tandem runs Instead, individual acceptance thresholds revealed itself to from the old nest to the new (forward tandem runs), in be the most parsimonious explanation (Robinson et al., Temnothorax sp., there are reverse tandem runs that start in 2009; Robinson et al., 2011). In effect, nests do compete for the new nest and recruit ants back to old nest (Pratt, 2008). scouts, but individual scouts make a decision on whether to Modelling by Planque´ et al. (2007) and later experimental commit to or keep searching for new nests in response to a work by Franks et al. (2009) started to explore the function nest’s quality rather than just taking longer to recruit to a of reverse tandem runs (Planque´ et al., 2007; Franks et al., poorer nest. In this way, a low quality nest is less likely to 2009). Like forward tandem runs, that induce followers get recruiters than a high quality nest. In addition, it may be from the old nest into becoming active recruiters, reverse that an scouts decision to commit to recruiting to a new nest tandem runs activate ants at the new nest, which have either may also be influenced by nestmates or their cues in the new been carried there, are currently inactive or have found it nest. Reverse tandem runs may also play an important role themselves. It has been suggested that reverse tandem runs in multiple nest choices, if workers are recruiting to more 123 4 E. L. Franklin than one nest. In this case, reverse tandem runs could be the first case of non-human teaching to be empirically used to reinforce recruitment to the better option. However, shown to fulfil all of Caro and Hauser’s (1992) criteria and we know little on the role of tandem runs (forward or continues to be one of the most rigorous studies of teaching reverse) in colony consolidation to one nest when they have in the laboratory environment. Franks and Richardson initially recruited to multiple choices (Mallon et al., 2001). (2006) showed bi-directional feedback between leader and Although it is reaching the quorum, not tandem running follower, keeping the pair together and progressing towards that is the point of choice in colony decision making, tan- the goal. They also showed that when a pair became sepa- dem running can be important to the colony’s collective rated, leaders wait for followers and followers search for decision making. Tandem running links the actions of their leader, but what happens if the pair cohesive interac- individual decision making scouts to assist in the collective tions between the pair fail? decision making of the whole colony. Tandem running is (1) When a leader loses contact with her follower she will just one of the behaviours that are important in the non- wait, but for how long do leaders invest in waiting for centralised organisation within ant colonies. Studies into stimulus from a follower? Richardson et al. (2007) provide non-centralised opinion polling and those exploring how a us with an answer, by taking away a leader’s follower in few informed individuals can influence the many have given different situations they could show that leading ants change us insights into how independently functioning units are their waiting times depending on a number of factors linked in other collective systems; for example in swarms (Richardson et al., 2007). Leaders were shown to be sensi- and even brains (Franks et al., 2002; Couzin et al., 2005; tive to the environment, waiting longer for followers when Marshall et al., 2009; Trianni et al., 2011). Using emigra- the quality of the nest to which they were recruiting was tions in the house-hunting ants as a model that can be high. They were sensitive to the progression of the tandem manipulated, hypotheses of self-organising, non-centralised run, waiting longer for followers, the longer the tandem run information processing can be tested. had progressed. They were also sensitive to their follower, waiting less time for followers with only one antenna. This could be because a follower with one antenna stimulates the Communication and teaching leader less, which results in the leader waiting less time. It could also be a mechanism to ‘give up’ on less efficient Meanwhile, studies were investigating within the tandem followers, that take longer to recruit, is that the leader can run interaction to expand the understanding of communi- invest in the best followers for future information transfers cation and social learning in Temnothorax sp. In a tandem (this is discussed in more detail later in this review). This run the leader guides a follower to a new nest or food, study suggests that leaders evaluate their investment in stopping if the follower loses contact. Franks and Richard- tandem run recruitment, only ‘giving up’ when it is more son (2006) explored the mechanics of tandem running and profitable to try recruiting again. Therefore, it is clear the discovered that there was intricate bi-directional feedback ants’ have sophisticated mechanisms with multiple inputs in between the leader and follower in the ant Temnothorax place to evaluate their investment in social learning though albipennis. The nature of the bi-directional feedback was tandem running. important as it demonstrated that the leader of the tandem (2) When a follower is separated from her leader she pair was not just ‘broadcasting’ but changing its behaviour will enter a search behaviour, looking to reunite her with in response to the follower. In addition, they showed that the her leader but for how long do followers search? In the behaviour of the leader in tandem running constitutes event the leader is not found where should the follower go teaching, by Caro and Hauser’s (1992) definition ‘‘An next? Should she either keep searching for a possible target individual actor A can said to teach if it modifies its or go back to the nest from which she was led? Franks et al. behaviour only in the presence of a naive observer B, at (2010) have begun to answer these questions. By interrupting some cost or at least no immediate benefit for itself. A’s tandem runs on the way to a new nest, by removing leaders behaviour, thereby, encourages or punishes B’s behaviour, or followers, they were able to examine the behaviour of a or provides B with experience, or sets an example for B. As follower after losing her leader. They showed that followers a result B acquires knowledge or learns a skill earlier in life search for almost exactly the time that a leader would wait in or more rapidly or efficiently than it might otherwise do, or the same situation. After a follower has stopped her inten- that B would not learn at all’’ (Caro and Hauser, 1992). sive local search she switches to a super diffusive (a wider Tandem running fulfils these criteria as it only occurs when random walk pattern that will take the follower away more an ant is being recruited and that it is much slower, by a rapidly from her start point) search, which may take her to a factor of 3, than its alternative, carrying. In addition, ants goal or reunite her with her leader. There is also some that follow tandem runs can find the nest faster than they evidence for path extrapolation from the followers, giving would do by individual exploration. Tandem running was value to partial tandem runs, with 21 % of followers (who 123 The journey of tandem running: the twists, turns and what we have learned 5 have lost their leader) going on to find the new nest alone The success of tandem runs can impact on colony fitness (Franks et al., 2010). Franks et al. (2010) show that fol- through decision making and food acquisition (Franks and lowers were more likely to find the new nest if they lost their Richardson, 2006). With this in mind, it may be beneficial to leader closer to the new nest. They suggest that the overall the colony to have experienced ants in the role of tandem direction taken by a follower is influenced by the partial run leader. This could either be because they have more tandem run which they had followed. They showed that the navigational experience or they have more experience in majority of the steps in the former follower’s paths, in the initiating and maintaining pair cohesion during a tandem 5 min following the breakup of the tandem run, were ori- run. With the question in the title ‘Do ants have to be old and entated in the same direction of the partial tandem run. The experienced to teach? Franklin et al. (2012) explored the idea that followers could be extrapolating paths from partial role of experience in tandem run participation and effi- tandem interactions is an intriguing one. It is possible that ciency. Their study was conducted using young inexperi- the ants could be finding the new nest by chance after their enced workers (with no tandem run experience), older switch to a wider, super diffusive search pattern triggered by inexperienced workers (with no tandem run experience) and the stimulation that a tandem run provides. However, if ants old experienced workers (with recent tandem run experi- are indeed extrapolating from tandem runs, then tandem ence). Their results suggest that although older experienced runs must be in some way providing the follower with a workers have a greater propensity to lead tandem runs, the heading or average trajectory. Route extrapolation has been ability to lead or follow successful tandem runs is present in shown by Franks et al. (2010) in a small number of ants in a all groups. They also found differences between young small arena but further work is needed to find out if inexperienced and older experienced workers’ tandem runs extrapolation is indeed happening and if it is, the mecha- when it came to efficiency measures; young workers dis- nisms behind it (Franks et al., 2010). If it can be shown that persed faster but older experienced workers are were more route extrapolation is being performed by the ants, then it accurate (Franklin et al., 2012). Older experienced workers could be assumed that tandem running provides followers may have greater accuracy due to having increased navi- with a continuous update of heading direction rather than gational experience. Unfortunately it cannot be confirmed just a location point to get to. whether it is speed, accuracy or another factor is more The following experiments tackle the question of what important for the learning of the follower in a tandem run. In ants are learning when participating in a tandem run. I begin this experiment successive tandem runs (where the follower with a study that explores the effect of visual impairment on of a tandem went on to be the leader of a subsequent tandem tandem running (Franklin et al., 2011). This study used paint run) were rare so they were unable to assess what and how to blinker T. albipennis workers, visually impairing them well the follower learnt during the tandem run. and then putting them in an emigration scenario in which Finally Franklin and Franks (2012) have identified some tandem running was required. In this case, the eyes of the of the information transferred in a tandem run. They did this ants had at least 90 % of the ommatidia covered with thick by comparing the ‘lesson learnt’ where a worker followed a black paint. The authors describe the ants as visually leader to a new nest and the ‘lesson taught’ the tandem the impaired as they could not be completely certain the ants’ follower went on to lead. They showed that: (1) the ants vision was completely removed. The results suggested that were not learning the route of their leader. This is mirrored visually impaired ants took part when there were many by the findings of Franks and Richardson (2006) where their unimpaired individuals present and even more surprisingly, followers of tandem runs did not return back to the nest on visual impairment did little to affect whether ants followed the route their leader had taken them. (2) The tandem routes tandem runs. However, it was shown that workers were less taken by the follower were not straighter or quicker than likely to lead tandems if visually impaired. Even when both their leader; unless they explored independently before leader and follower were blinkered, they showed little dif- going on to lead a tandem run themselves. This was the ference in tandem run speeds or path straightness. Franklin same for workers who found the nest independently that et al. (2011) suggest that the ants were able to use other went on to lead tandem runs. To summarise, tandem running mechanisms such as olfaction and path integration to nav- provides the follower with the opportunity to gain knowl- igate, instead of predominantly vision (Aron et al., 1988; edge on how to get to a location but not a prescribed route or Mu¨ller and Wehner, 1988). However, the effectiveness of a path to improve on. the information transfer (how to locate the new nest site) So what are workers using to learn the location of a new during the tandem run was not tested in this experiment as nest or food? I suggest the following workers are learning former followers were removed after their following bout the location of new nests by predominantly using path and not allowed to become leaders of successive tandem integration (Mu¨ller and Wehner, 1988), an accumulator that runs (Franklin et al., 2011). logs the distance and direction from a start point. They then

123 6 E. L. Franklin use visual landmarks when improving routes independently as teaching difficult. Perhaps: there are two main reasons for and leading tandem runs (Pratt et al., 2001; McLeman et al., this reluctance to define tandem running as teaching. The 2002). This could explain why visually impaired ants are first concerns the nature of teaching and the second concerns more likely to follow but are less likely to lead tandem runs with the information transferred during the tandem run. (Franklin et al., 2011). It also may explain why the more I do not wish to go into the details of the theories of teaching accurate older experienced ants with greater navigation in non-human in this paper but instead direct experience are more likely to lead tandem runs (Franklin those interested to several excellent reviews on the subject et al., 2012) (Leadbeater et al., 2006; Thornton et al., 2007; Hoppitt If tandem runs are so slow and they do not communicate et al., 2008; Thornton and Raihani, 2008) As humans, we a route to follow or improve on, why do the ants use them? tend to think of teaching as helping an individual to develop The workers could just explore independently and when or filling in a deficit in their knowledge. However, in social recruiting to a nest, switch to carrying when the quorum insects such as T. albipennis ants, the benefit gained from number is met but in many situations they invest in tandem teaching is to the whole colony through inclusive fitness i.e. running. There are two main reasons that can be distilled the whole colony. Therefore, it is useful to think of the from the tandem running literature: first, tandem runs, teaching identified in ants like a family company teaching ‘recruit recruiters’ (Mo¨glich, 1978), so that a worker that its employees how to use a new piece of equipment. follows a tandem run can become active in recruiting others. Teaching an individual in this case does not directly benefit This does not happen when a worker is carried; either the individual, but if many workers can learn how to use because the carried worker is not given the opportunity to the piece of equipment, the company’s productivity will walk and learn the way, due to having an inverted carrying increase and ultimately increase employee wages and ben- position, or is not stimulated into being active in the emi- efit to kin. Looking at it in this way, the ant’s evaluation, gration. Second, tandem running speeds up the flow of being able to give up on poorer learners makes sense. If an information about the location of a new resource through the employee is struggling to learn about the machinery, it colony when the resource is difficult to find independently. makes sense not to train them and train someone who learns If workers can find the nest easily by independent explo- faster. In this way the company would be evaluating its ration they do not use tandem running (Pratt et al., 2002). A investment in teaching, in a similar manner to the ant col- similar switch happens in honeybees (Apis mellifera), if ony. The difference between the company and the ant colony, floral resources are easy to find, foragers follow fewer is that in Temnothorax ants, there are exquisite algorith- waggle dances i.e. bees use more independent than social mic mechanisms that have evolved, providing a means information (Seeley, 1983). Tandem running also links the to evaluate teaching investment, without the invoking actions of individual scouts to allow colonies to make col- theory of mind. Thus, maximising effect but minimising cost lective decisions when new nests are hard for workers to to the colony. There are two reasons why the definition of find independently. tandem running as teaching are debated. There is the argu- By following a tandem run a worker gets the opportunity ment made by some that the Caro and Hauser definition of to learn how to get from one location to another. However, teaching needs some criteria as to the type of information trans- evidence from recent experiments suggests that the infor- ferred (Hoppitt et al., 2008). They argue that any definition mation is not in the form of a prescribed route to follow, or of teaching should be reserved for the transfer of skills or indeed to be improved on (Franklin and Franks, 2012). Yet, rules rather than a declaration of fact. The other reason during a tandem run a follower learns how to get to the hinges on whether tandem running is ‘telling’ the follower target and, because this is actively facilitated by the leader, the location or something more (Leadbeater et al., 2006). tandem running has been defined as teaching. The interac- Franks and Richardson (2006) showed that the leader changes tion between a leader and a follower in a tandem running her behaviour in response to the follower’s actions, differing differs from forms of broadcast information, such as pher- it from ‘broadcasting’, as in pheromone trails. The argument omone trails, as the leader responds to the follower’s is whether those bi-directional interactions actually give actions. In addition, colonies evaluate the best strategy to the follower information, such as a trajectory, assisting the use for emigrations ensuring they only invest in tandem learning of the follower, or they simply function to keep running when they need to. All of these mechanisms provide the pair together. Those who argue that the evidence sug- the basis for tandem running to occur, maximising its benefit gests that tandem running involves just ‘telling’ state that: to the colony, without a theory of mind. Tandem running has (1) Following ants are given the opportunity to learn how to provided substantial evidence to be defined as teaching by get to a location (either through path integration or land- Caro and Hauser’s (1992) definition. However, some con- marks), (2) that followers learn the value of the target on sider the Caro and Hauser (1992) definition is in some way personal exploration and this is akin to being informed of a lacking and therefore find the description of tandem running location by being led there, (3) the bi-directional feedback 123 The journey of tandem running: the twists, turns and what we have learned 7 between tandem runners just maintains pair cohesion and Beckers R., Goss S., Deneubourg J.L. and Pasteels J.M. 1989. Colony transfers no navigational information. size communication and ant foraging strategy. Psyche 96: 239-256 Buschinger A., Ehrhardt W. and Winter U. 1980. The organization of However, there are those who think there is already slave raids in dulotic ants, a comparative study. Z. Tierpsychol. - overwhelming evidence for the classification of tandem J. Comp. Ethol. 53: 245-264 running as teaching from the evaluation, tandem interac- Buschinger A. and Winter U. 1977. Recruitment of nestmates by tions and tandem path extrapolation. There is tantalising tandem running during slave-raids of the dulotic ant, Harpago- xenus sublaevis (Nyl.). . Soc. 24:183-190 evidence that may suggest that tandem running is more than Caro T.M. and Hauser M.D. 1992. Is there teaching in nonhuman a means to communicate location. One such piece of evi- animals? Quart. Rev. Biol. 67: 151-174 dence is the possible path extrapolation shown by the Couzin I.D., Krause J., Franks N.R. and Levin S.A. 2005. Effective followers of partial tandem runs. If ants are indeed extra- leadership and decision-making in groups on the move. Nature 433: 513-516 polating from partial tandem runs, then information about Farina W.M., Gru¨ter C. and Dı´az P.C. 2005. Social learning of floral either a trajectory or the orientation must be conveyed odours inside the honeybee hive. Proc. R. Soc. Lond. B. 272: before the completion of the tandem run. There is also the 1923-1928 possibility that tandem running gives the follower some idea Franklin E.L. and Franks N.R. 2012. Individual and social learning in tandem running recruitment by ants. Anim. Behav. 84: 361-368 of the quality of the target. When foraging for food, troph- Franklin E.L., Robinson E.J.H., Marshall J.A.R., Sendova-Franks A.B. allaxis could be coupled with tandem running to provide this and Franks N.R. 2012. Do ants need to be old and experienced to information (Farina et al., 2005). In searching for a new nest teach? J. Exp. Biol. 215: 1287-1292 site, leader urgency or the fact she recruited at all could be Franklin E.L., Richardson T.O., Sendova-Franks A.B., Robinson E.J.H. and Franks N.R. 2011. Blinkered teaching: tandem running giving the follower information about the new nest site’s by visually impaired ants. Behav. Ecol. Sociobiol. 65: 569-579 quality. Experiments that could provide further information Franks N.R., Richardson T.O., Keir S., Inge S.J., Bartumeus F. and to support the learning opportunity hypothesis would be Sendova-Franks A.B. 2010. Ant search strategies after interrupted very revealing. However tandem running’s classification as tandem runs. J. Exp. Biol. 213: 1697-1708 Franks N.R., Dechaume-Moncharmont F.X., Hanmore E. and Rey- teaching is considered, evidence from further research is nolds J.K. 2009. Speed versus accuracy in decision-making ants: required and I for one, think currently we are only just expediting politics and policy implementation. Proc. R. Soc. ‘scratching the surface’ of the information that is transferred Lond. B. 364: 845-852 within a tandem run. Franks N.R., Hardcastle K.A., Collins S., Smith F.D., Sullivan K.M.E., Robinson E.J.H. and Sendova-Franks A.B. 2008. Can ant colonies This review has given a documentation of the scientific choose a far-and-away better nest over an in-the-way poor one? journey taken by those who have investigated tandem run- Anim. Behav. 76: 323-334 ning, from the first description of tandem running through Franks N.R., Dornhaus A., Metherell B.G., Nelson T.R., Lanfear S.A.J. its use as an experimental tool to explore social learning and and Symes W.S. 2006. Not everything that counts can be counted: ants use multiple metrics for a single nest trait. Proc. R. Soc. Lond. the ongoing philosophical debates it has stimulated about B. 273: 165-169 the meaning of teaching. Tandem running experiments have Franks N.R. and Richardson T. 2006. Teaching in tandem-running given us fundamental insights into collective decision ants. Nature 439: 153-153 making, learning and even teaching and continue to do so as Franks N.R., Mallon E.B., Bray H.E., Hamilton M.J. and Mischler T.C. 2003. Strategies for choosing between alternatives with different new research is released. attributes: exemplified by house-hunting ants. Anim. Behav. 65: 215-223 Acknowledgments I want to thank Professor Nigel Franks, Dr Franks N.R., Pratt S.C., Mallon E.B., Britton N.F. and Sumpter D.J.T. Daphna Gottlieb and Norasmah Basari in the ant lab, University of 2002. Information flow, opinion polling and collective intelli- Bristol for their thought provoking debates and comments which gence in househunting social insects. Proc. R. Soc. Lond. B. 35: enabled me to develop my own conclusions presented in this review. I 1567-1583 also want to give special thanks to Dr Liz Langridge for her thorough Fresneau D. 1985. Individual foraging and path fidelity in a ponerine and thought provoking review and Duncan Bates and Tom Unsworth ant. Insect. Soc. 32: 109-116 for their assistance with proofing. Hingston R.W.G. 1929. Instinct and Intelligence. McMillan & Co. New York. Ho¨lldobler B., Mo¨glich M. and Maschwitz U. 1974. Communication by tandem running in the ant Camponotus sericeus. J. Comp. References Physiol. 90: 105-127 Ho¨lldobler B. and Traniello J. 1980. Tandem running pheromone in Agbogba C. 1984. Tandem running behavior in two species of ponerine ants. Naturwissenschaften 67: 360-360 ponerine ants Mesoponera caffraria (Smith) and Hypoponera sp. Ho¨lldobler B. 1971. Recruitment behaviour in Camponotus socius (Hym. Formicidae). Insect. Soc. 31: 264-276 (Hym. Formicidae). Z. vergl. Physiol. 75: 123-142 Adlerz G. 1986. Myrmecologiska studier III. Tomognathus sublaevis Hoppitt W.J.E., Brown G.R., Kendal R., Rendell L., Thornton A., Mayr. Bihang Till K. Svenska Vet-Akad. Handingar 21: 1-76 Webster M.M. and Laland K.N. 2008. Lessons from animal Aron S., Deneubourg J.L. and Pasteels J.M. 1988. Visual cues and trail teaching. Trends Ecol. Evol. 23: 486-493 following idiosyncrasy in Leptothorax unifasciatus an orientation Jessen K. and Maschwitz U. 1986. Orientation and recruitment process during foraging. Insect. Soc. 35: 355-366 behavior in the ponerine ant Pachycondyla tesserinoda (Emery)

123 8 E. L. Franklin

laying of individual specific trails during tandem running. Behav. Pratt S.C., Brooks S.E. and Franks N.R. 2001. The use of edges in Ecol. Sociobiol. 19: 151-155 visual navigation by the ant Leptothorax albipennis. Ethology Langridge E.A., Franks N.R. and Sendova-Franks A.B. 2004. 107: 1125-1136 Improvement in collective performance with experience in ants. Pratt S.C., Mallon E.B., Sumpter D.J.T. and Franks N.R. 2002. Behav. Ecol. Sociobiol. 56: 523-529 Quorum sensing, recruitment, and collective decision-making Lane A.P. 1977. Tandem running in Leptothorax uniasciatus (For- during colony emigration by the ant Leptothorax albipennis. micidae, Myrmicinae); New data concerning recruitment and Behav. Ecol. Sociobiol. 52: 117-127 orientation in this species. IUSSI Int. Congr. IUSSI Wageningen. Pratt S.C. 2008. Efficiency and regulation of recruitment during colony pp 65-66 emigration by the ant Temnothorax curvispinosus. Behav. Ecol. Leadbeater E., Raine N.E. and Chittka L. 2006. Social learning: Ants Sociobiol. 62:1369-1370 and the meaning of teaching. Curr. Biol. 16: 323-325 Richardson T.O., Houston A.I. and Franks N.R. 2007. Teaching with Liefke C., Holldobler B. and Maschwitz U. 2001. Recruitment evaluation in ants. Curr. Biol. 17: 1520-1526 behavior in the ant genus Polyrhachis (, Formici- Robinson E.J.H, Franks N.R., Ellis S., Okuda S. and Marshall J.A.R. dae). J. Insect Behav. 14: 637-657 2011. A simple threshold rule is sufficient to explain sophisticated Mailleux A.C., Deneubourg J.L. and Detrain C. 2003. How does collective decision-making. PloS one 6: e19981 colony growth influence communication in ants? Insect. Soc. 50: Robinson E.J.H., Smith F.D., Sullivan K.M.E. and Franks N.R. 2009. 24-31 Do ants make direct comparisons? Proc. R. Soc. Lond. B. 276: Mallon E.B., Pratt S.C. and Franks N.R. 2001. Individual and 2635-2641 collective decision-making during nest site selection by the ant Seeley T.D. 1983 Division of labor between scouts and recruits in Leptothorax albipennis. Behav. Ecol. Sociobiol. 50: 352-359 honeybee foraging. Behav. Ecol. Sociobiol. 12: 253-259 Mallon E.B. and Franks N.R. 2000. Ants estimate area using Buffon’s Stuart R.J. 1986. An early record of tandem running in Leptothoracine needle. Proc. R. Soc. Lond. B. 267: 765-770 ants Gottfrid Adlerz 1896. Psyche 93: 103-106 Marshall J.A.R., Bogacz R., Dornhaus A., Planque´ R., Kovacs T. and Sumpter D.J.T. and Brannstrom A. 2008. Synergy in social commu- Franks N.R. 2009. On optimal decision-making in brains and nication. In: Sociobiology of Communication: an Interdisci- social insect colonies. J. R. Soc. Interface 6: 1065-1074 plinary Perspective (d’Ettorre P. and Hughes D.P., Eds). Oxford Maschwitz U., Ho¨lldobler B. and Mo¨glich M. 1974. Recruitment by tan- University Press, Oxford. pp 191-208 dem running in the ant Bothroponera tesserinoda. Z. Tierpsychol. Thornton A. and Raihani N.J. 2008. The evolution of teaching. Anim. 35: 113-123 Behav. 75:1823-1836 McLeman M.A., Pratt S.C. and Franks N.R. 2002. Navigation using Thornton A., Raihani N.J. and Radford A.N. 2007. Teachers in the visual landmarks by the ant Leptothorax albipennis. Insect. Soc. wild: some clarification. Trends Cogn. Sci. 11: 272-273 49: 203-208 Trianni V., Tuci E., Passino K.M. and Marshall J.A.R. 2011. Swarm Mo¨glich M. and Ho¨lldobler B. 1974. Social carrying behavior and cognition: an interdisciplinary approach to the study of self- division of labor during nest moving in ants. Psyche 81: 219-236 organising biological collectives. Swarm Intelligence 5: 3-18 Mo¨glich M. 1978. Social-organization of nest emigration in Lepto- Wheeler W. 1908. The ants of Puerto Rico and the Virgin Islands. Bull. thorax (Hym Form). Insect. Soc. 25: 205-225 Amer. Mus. Nat. Hist. 24: 117-158 Mu¨ller M. and Wehner R. 1988. Path integration in desert ants, Wilson E.O. 1959. Communication by tandem running in the ant genus Cataglyphis fortis. Proc. Natl Acad. Sci. U.S.A. 85: 5287-5290 Cardiocondyla. Psyche 66: 29-34 Planque´ R., van den Berg J.B. and Franks N.R. 2010. Recruitment Wilson E.O. 1971. The Insect Societies. Belknap, Cambridge. strategies and colony size in ants. PLoS One 5: e11664 Planque´ R., Dechaume-Moncharmont F.X., Franks N.R., Kovacs T. and Marshall J.A.R. 2007. Why do house-hunting ants recruit in both directions? Naturwissenschaften 94: 911-918

123