Waste management in the leaf-cutting ant Acromyrmex echinatior: the role of worker size, age and plasticity

Division of labour is the hallmark of the success of many social animals. It may be especially important with regard to waste management because waste often contains pathogens or hazardous toxins and worker specialisation can reduce the number of group members exposed to it. Here we examine waste management in a fungus-farming, leaf-cutting ant, Acromyrmex echinatior, in which waste management is necessary to protect their vulnerable fungal crop. By marking ants with task-specific paint colours, we found clear division of labour between workers that engage in waste management and those that forage, at least during the fine timescale of the 3-day marking period. This division of labour was influenced by both age and size, with waste management workers tending to be smaller and younger than foragers. The role of preventing contaminated ants from entering the colony was fulfilled mainly by medium-sized workers. When the level of waste was experimentally increased, most of the ants that responded to remove the waste were workers previously engaged in tasks inside the nest rather than external waste workers or foragers. These responding workers tended to be young and medium-sized. Surprisingly, the responding ants were subsequently able to revert back to working within the fungus garden, but the probability of them doing so depended on their age and the length of time they were exposed to waste. The results demonstrate the importance of division of labour with regard to waste management in A. echinatior and show that this is adaptable to changing needs.     

Division of labour and worker size polymorphism in ant colonies: the impact of social and genetic factors

Division of labour among workers is central to the organisation and ecological success of insect societies. If there is a genetic component to worker size, morphology or task preference, an increase in colony genetic diversity arising from the presence of multiple breeders per colony might improve division of labour. We studied the genetic basis of worker size and task preference in Formica selysi, an ant species that shows natural variation in the number of mates per queen and the number of queens per colony. Worker size had a heritable component in colonies headed by a doubly mated queen (h ²=0.26) and differed significantly among matrilines in multiple-queen colonies. However, higher levels of genetic diversity did not result in more polymorphic workers across single- or multiple-queen colonies. In addition, workers from multiple-queen colonies were consistently smaller and less polymorphic than workers from single-queen colonies. The relationship between task, body size and genetic lineage appeared to be complex. Foragers were significantly larger than brood-tenders, which may provide energetic or ergonomic advantages to the colony. Task specialisation was also often associated with genetic lineage. However, genetic lineage and body size were often correlated with task independently of each other, suggesting that the allocation of workers to tasks is modulated by multiple factors. Overall, these results indicate that an increase in colony genetic diversity does not increase worker size polymorphism but might improve colony homeostasis.     

Worker size-related task partitioning in the foraging strategy of a seed-harvesting ant species

Messor bouvieri is a seed-harvesting ant species in which workers forage in trails from the nest to a search area. A previous observation of seed transfer events between workers returning to the nest suggested potential task partitioning. In this study, we describe seed transportation and analyze the role of task partitioning in the foraging strategy of this species in terms of seed intake efficiency in relation to costs and benefits based on transport speed and task reliability. We assess the harvesting efficiency of task partitioning by comparing cooperative seed transport (CST) and individual seed transport (IST) events. Our results show task partitioning in the form of a sequence of transfer events among workers going from the search area to the nest. Importantly, and despite the weak worker polymorphism of this species, this sequence involved workers of different sizes, with seeds usually being passed along from smaller to larger workers. In addition, we show that small workers are better at finding seeds (spend less time finding a seed), and large workers are better at transporting them (were faster when walking back to the nest and lost fewer seeds). However, we failed to demonstrate that workers of different sizes are specialized in performing the task in which they excel. Overall, sequential CST in M. bouvieri results in a greater seed intake because seed search time decreases and task reliability increases, compared to IST. The determinants and adaptive benefits of CST are discussed.     

Why do not all workers work? Colony size and workload during emigrations in the ant Temnothorax albipennis

Here, we study distribution of workload and its relationship to colony size among worker ants of Temnothorax albipennis, in the context of colony emigrations. We find that one major aspect of workload, number of items transported by each worker, was more evenly distributed in larger colonies. By contrast, in small colonies, a small number of individuals perform most of the work in this task (in one colony, a single ant transported 57% of all items moved in the emigration). Transporters in small colonies carried more items to the new nest per individual and achieved a higher overall efficiency in transport (more items moved per transporter and unit time). Our results suggest that small colonies may be extremely dependent on a few key individuals. In studying colony organisation and division of labour, the amount of work performed by each individual, not just task repertoire (which tasks are performed at all), should be taken into account.     

Predator recognition and evasive behavior by sweat bees, <Emphasis Type="Italic"> Lasioglossum umbripenne </Emphasis>(Hymenoptera: Halictidae), in response to predation by ants, <Emphasis Type="Italic"> Ectatomma ruidum </Emphasis>(Hymenoptera: Formicidae)

Ectatomma ruidum is an abundant soil-nesting Neotropical ant, which displays extensive behavioral flexibility during foraging activities. We studied here one unusual element of their behavioral repertoire: ambush predation. A worker of E. ruidum waits near a nest of a social sweat bee, Lasioglossum umbripenne, lunging at incoming bees, or less frequently, at departing bees. However, bees detected ambushing ants and modified their behavior. Dead ants placed at bees' nest entrances significantly decreased bee activity, indicating that bees recognized dead ants as potential predators. Neither simple black models (square and rectangle) nor olfactory cues had any effect on overall bee activity. A returning bee usually approached her entrance and immediately entered, but if an ant was waiting at the nest, a bee was significantly more likely to abort the first approach flight and then to re-approach the nest on the side opposite the ant's position. As models became increasingly ant-like, returning bees more frequently aborted their first approach flight, expressing other behaviors before entering nests. These behaviors included withdrawal followed by an approach from a different direction; zigzagging flights, either from a distance or close to the entrance or even a close inspection; landing a short distance from the nest, then approaching on foot or waiting for several seconds before entering. Ants responded with effective counter-behaviors. Behavioral flexibility in nest entering/exiting by L. umbripenne and in hunting strategy by E. ruidum shows the complexity of this predator-prey relationship, and illustrates the importance of information processing by both species involved in determining the outcome of the interspecific interaction.     

Worker policing and worker reproduction in Apis cerana

Workers of the Asian hive bee, Apis cerana, are shown to have relatively high rates of worker ovary activation. In colonies with an active queen and brood nest, 1-5% of workers have eggs in their ovarioles. When A. cerana colonies are dequeened, workers rapidly activate their ovaries. After 4 days 15% have activated ovaries and after 6 days, 40%. A cerana police worker-laid eggs in the same way that A. florea and A. mellifera do, but are perhaps slightly more tolerant of worker-laid eggs than the other species. Nevertheless, no worker's sons were detected in a sample of 652 pupal males sampled from 4 queenright colonies. A cerana continue to police worker-laid eggs, even after worker oviposition has commenced in a queenless colony.     

Testing the limits of social resilience in ant colonies

Social resilience is the ability of Leptothorax ant colonies to re-assemble after dissociation, as caused, for example, by an emigration to a new nest site. Through social resilience individual workers re-adopt their spatial positions relative to one another and resume their tasks without any time being wasted in worker respecialisation. Social resilience can explain how an efficient division of labour can be maintained throughout the trials and tribulations of colony ontogeny including the, often substantial, period after the queen dies when the ability to conserve worker social relationships may be essential for efficiency to be maintained. The mechanism underlying social resilience is, therefore, expected to be robust even in the absence of many of the colony’s components, such as the queen, the brood and even a large proportion of the workers. Such losses are likely, given the ecology of this genus. Using sociotomy experiments, we found that social resilience can occur in the absence of the queen. Furthermore, the spatial component of social resilience can occur even when the queen, the brood, as well as a large proportion of the workers, are all absent simultaneously and hence many of the tasks are missing. We conclude, therefore, that social resilience is indeed robust. This does not, however, preclude worker flexibility in response to changes in task supply and demand. We propose a possible sorting mechanism based on worker mobility levels which might explain the robustness underlying this phenomenon. Received: 25 October 1999 / Accepted: 1 April 2000     

Dominance orders,worker reproduction,and queen-worker conflict in the slave-making ant Harpagoxenus sublaevis

Summary In a queenright colony of the monogynous slave-making ant Harpagoxenus sublaevis, a subset of workers formed a linear dominance order in which dominance was corrlated with ovarian development, frequency of trophallaxis, length of time spent in the nest, but not body size. Identical dominance orders occurred in queenless colonies. Experiments in which the top-ranking workers were removed from queenless colonies demonstrated that worker dominance behaviour inhibits egg-laying in subordinates. A similar removal experiment showed queens restrict dominance behaviour and egg-laying in workers, probably pheromonally. Observations of slave raids indicated ovary-developed workers spent significantly less time scouting for slaves, and tended to participate less in slave raids, than workers without ovarian development. These findings suggest that potentially fertile H. sublaevis workers aggressively compete for egg-laying rights, consume extra food for egg development, and safeguard their reproductive futures by avoiding risks outside the nest. Hence worker reproduction in this species strongly influences the colony's social structure, nutrient flow, and division of labour, even though all workers in a colony are full sisters. I hypothesize that worker reproduction was formerly even more prevalent in H. sublaevis, with workers following the strategy of raising sisters and producing sons predicted by kinship theory. Its continued existence despite queen opposition conceivably results from selection on orphaned workers to reproduce, and the inability of slave-maker workers to raise female-biased broods. The social organization of H. sublaevis therefore highlights the importance both of worker reproduction and of the concomitant queen-worker conflict over male parentage in Hymenopteran social evolution.     

Serial polygyny and colony genetic structure in the monogynous queenless ant Diacamma cyaneiventre

Serial polygyny, defined as the temporal succession of several reproductive females in a colony, occurs in some monogynous social insects and has so far attracted little attention. Diacamma cyaneiventre is a queenless ponerine ant found in the south of India. Colonies are headed by one singly mated worker, the gamergate. After the death of the gamergate or her absence following colony fission, the gamergate is replaced by a newly eclosed nestmate worker. After a replacement, colonies go through short-lived periods in which two matrilines of sisters co-occur. This is a situation which can be described as serial polygyny. To measure the consequences of serial polygyny, a genetic analysis was performed on 449 workers from 46 colonies of D. cyaneiventre using five microsatellite loci. The presence of more than one matriline among workers of the same nest was detected in 19% of colonies, indicating a recent change of gamergate. The average genetic relatedness among nestmate workers was 0.751 and did not significantly differ from the theoretical expectation under strict monogyny and monandry (0.75). A simple analytical model of the temporal dynamics of serial polygyny was developed in order to interpret these results. We show that the rate of gamergate turnover relative to the rate of worker turnover is the crucial parameter determining the level of serial polygyny and its effect on the genetic structure of colonies. This parameter, estimated from our data, confirms that serial polygyny occurs in D. cyaneiventre but is not strong enough to influence significantly the average genetic relatedness among workers.     

Cuticular hydrocarbons and reproductive status in the social wasp Polistes dominulus

Most species of social insect are characterized by a reproductive division of labor among morphologically specialized individuals. In contrast, there exist many species where all individuals are morphologically identical and dominance relationships determine which individuals mate and/or reproduce. In newly founded multiple-foundress associations of the social wasp Polistes dominulus, foundresses establish dominance hierarchies where the top-ranked (alpha) female monopolizes egg laying. The possibility that chemical cues are used for recognition of egg-laying individuals has not been explored in this wasp. Using non-destructive techniques, we examined the relationship between ovarian activity and the proportions of cuticular hydrocarbons of three female types (dominant and subordinate foundresses and workers) in 11 colonies. Immediately after nest foundation, no differences were found between alpha and subordinate females. In contrast, at worker emergence, alpha females were statistically distinguishable from both subordinates and workers. We experimentally removed the alpha female in 5 of the original nests and reanalyzed hydrocarbon proportions of the new dominant individual. Replacement individuals were all found to acquire a cuticular signature characteristic of the alpha female. This suggests that cuticular hydrocarbons are used as cues of ovarian activity in P. dominulus, and we discuss our results in terms of a switch from behavioral dominance to chemical signaling in this wasp.     

Nest defense and early production of the major workers in the dimorphic ant Colobopsis nipponicus (Wheeler) (Hymenoptera : Formicidae)

Summary Production of the major subcaste and its contribution to nest survival in the dimorphic ant Colobopsis nipponicus was examined in the field. In this species, the first major workers were reared in the second brood, very early in the colony life cycle. A field experiment demonstrated that artificial colonies without major workers could not survive, whereas colonies with at least one major worker per nest entrance could. Because major workers of C. nipponicus defend the nest entrance by head plugging, the lack of nest defenders in the experimental colonies seemed to be a major cause of nest failure. The defensive value of major workers was much higher than that of minor workers. Many artificial colonies without major workers were displaced by competitors for nest sites, especially by those of other conspecific colonies. In addition, more than 90% of field colonies nested with other conspecific colonies on the same tree. The early production of major workers in C. nipponicus seemed to be very important for the survival of incipient colonies.     

Worker policing in the bee Apis florea

Apis florea is a single-combed, open-nesting, dwarf honeybee indigenous to Asia. In common with other species of this genus, A. florea is highly polyandrous, and is therefore predicted to curtail worker reproduction by mutual policing mechanisms that keep worker reproduction at an extremely low level. Policing mechanisms could involve destruction of workers' eggs or offspring, or aggression toward those workers that are reproductively active. We show that in A. florea, worker-laid eggs are eliminated approximately twice as fast as queen-laid eggs, indicating that A. florea uses oophagy of worker-laid eggs as a mechanism of worker policing. Genetic analysis of four colonies indicated that all males produced were sons of queens, not workers. Dissections of 800 workers, from four colonies, did not reveal any significant levels of ovary activation. These results suggest that worker policing is an effective component of the mechanisms that maintain worker sterility in this species. Furthermore, they suggest that worker policing via oophagy of worker-laid eggs is pleisiomorphic for the genus.     

Worker reproduction in honey-bees (Apis) and the anarchic syndrome: a review

Honey-bees, Apis, are an important model system for investigating the evolution and maintenance of worker sterility. The queen is the main reproductive in a colony. Workers cannot mate, but they can lay unfertilized eggs, which develop into males if reared. Worker reproduction, while common in queenless colonies, is rare in queenright colonies, despite the fact that workers are more related to their own sons than to those of the queen. Evidence that worker sterility is enforced by 'worker policing' is reviewed and worker policing is shown to be widespread in Apis. We then discuss a rare behavioural syndrome, 'anarchy', in which substantial worker production of males occurs in queenright colonies. The level of worker reproduction in these anarchic colonies is far greater than in a normal queenright honey-bee colony. Anarchy is a counterstrategy against worker policing and an example of a 'cheating' strategy invading a cooperative system.     

Transmission of a pathogen in Bombus terrestris,with a note on division of labour in social insects

Summary Parasites of social insect workers can be transmitted within the colony to other, related host individuals or, alternatively, to unrelated workers of other colonies. Division of labour affects the probability of transmission, as young individuals often work inside the nest whereas older ones often leave the nest to forage. Therefore, the relative probabilities of transmission within-vs. between-nests is also affected by the delay between host infection and the shedding of propagules, i.e. the latent period of the parasite strain. We therefore hypothesized that strains of the flagellate parasite Crithidia bombi (Trypanosomatidae, Zoomastigophorea) infecting workers of the bumble bee Bombus terrestris (Hymenoptera, Apidae) could differ in their delays and coexist in a population. This would be the case if strains that are shed after a short time delay were more efficiently transmitted to other colony members, whereas strains with long delays were more efficiently transmitted to non-related workers in the population. We tested this hypothesis by experimentally varying time delay and by allowing transmission to either sister workers from the same nest or unrelated workers from other nests. Transmission of C. bombi was measured as the number of parasitic cells shed by the exposed workers after a standard period. The results showed that relatedness as such had no effect, but that delay and nest identity were highly significant effects to explain variation in transmission success. There was a significant interaction between nest identity and delay, such that bees of some colonies acted as efficient transmitters for C. bombi under short delays and vice versa. We discuss how division of labour may affect parasitism in social insects and, vice versa, how division of labour may be under selection from the effects of parasitism, using available evidence from the literature. Correspondence to: P. Schmid-Hempel     

Competition and cooperation: bumblebee spatial organization and division of labor may affect worker reproduction late in life

Within-group conflict may influence the degree to which individuals within a group cooperate. For example, the most dominant individuals within a group often gain access to the best resources and may be less inclined to perform risky tasks. We monitored space use and division of labor among all workers in three colonies of bumblebees, Bombus impatiens, during the ergonomic and queenless phases of their colony cycle. We then measured the two largest oocytes in each worker to estimate each individual's reproductive potential at the end of the colony cycle. We show that workers that remained farther from the queen while inside the nest and avoided risky or more energy-expensive tasks during the ergonomic phase developed larger oocytes by the end of the colony cycle. These individuals also tended to be the largest, oldest workers. After the queen died, these workers were more likely than their nestmates to increase brood incubation. Our results suggest that inactive bumblebees may be storing fat reserves to later develop reproductive organs and that the spatial organization of workers inside the nest, particularly the distance workers maintain from the queen, may predict which individuals will later have the greatest reproductive potential in the colony.     

How is activity distributed among and within tasks in Temnothorax ants?

How social insect colonies behave results from the actions of their workers. Individual variation among workers in their response to various tasks is necessary for the division of labor within colonies. A worker may be active in only a subset of tasks (specialist), perform all tasks (elite), or exhibit no particular pattern of task activity (idiosyncratic). Here we examine how worker activity is distributed among and within tasks in ants of the genus Temnothorax. We found that workers exhibited elitism within a situation, i.e., in particular sets of tasks, such as those associated with emigrations, nest building, or foraging. However, there was weak specialization for working in a particular situation. A few workers exhibited elitism across all situations, i.e., high performance in all tasks in all situations. Within any particular task, the distribution of activity among workers was skewed, with few ants performing most of the work and most ants performing very little of the work. We further found that workers persisted in their task preference over days, with the same individuals performing most of the work day after day. Interestingly, colonies were robust to the removal of these highly active workers; they were replaced by other individuals that were previously less active. This replacement was not short-lived; when the removed individuals were returned to the colony, not all of them resumed their prior high activity levels, and not all the workers that replaced them reduced their activity. Thus, even though some workers specialize in tasks within a particular situation and are persistent in performing them, task allocation in a colony is plastic and colonies can withstand removal of highly active individuals.     

Weak specialization of workers inside a bumble bee (<Emphasis Type="Italic">Bombus impatiens</Emphasis>) nest

Division of labor is common across social groups. In social insects, many studies focus on the differentiation of in-nest and foraging workers and/or the division of foraging tasks. Few studies have specifically examined how workers divide in-nest tasks. In the bumble bee, Bombus impatiens, we have shown previously that smaller workers are more likely to feed larvae and incubate brood, whereas larger workers are more likely to fan or guard the nest. Here, we show that in spite of this, B. impatiens workers generally perform multiple tasks throughout their life. The size of this task repertoire size does not depend on body size, nor does it change with age. Further, individuals were more likely to perform the task they had been performing on the previous day than any other task, a pattern most pronounced among individuals who guarded the nest. On the other hand, there was no predictable sequence of task switching. Because workers tend to remain in the same region of the nest over time, in-nest workers may concentrate on a particular task, or subset of tasks, inside that region. This division of space, then, may be an important mechanism that leads to this weak specialization among in-nest bumble bee workers.     

Division of foraging labor in ants can mediate demands for food and safety

Solitary foragers can balance demands for food and safety by varying their relative use of foraging patches and their level of vigilance. Here, we investigate whether colonies of the ant, Formica perpilosa, can balance these demands by dividing labor among workers. We show that foragers collecting nectar in vegetation near their nest are smaller than are those collecting nectar at sites away from the nest. We then use performance tests to show that smaller workers are more likely to succumb to attack from conspecifics but feed on nectar more efficiently than larger workers, suggesting a size-related trade-off between risk susceptibility and harvesting ability. Because foragers that travel away from the nest are probably more likely to encounter ants from neighboring colonies, this trade-off could explain the benefits of dividing foraging labor among workers. In a laboratory experiment, we show that contact with aggressive workers results in an increase in the mean size of recruits to a foraging site: this increase was not the result of more large recruits, but rather because fewer smaller ants traveled to the site. These results suggest that workers particularly susceptible to risk avoid dangerous sites, and suggest that variation in worker size can allow colonies to exploit profitably both hazardous and resource-poor patches.Communicated by L. Sundström     

Dominance and polyethism in the eusocial wasp Mischocyttarus mastigophorus (Hymenoptera: Vespidae)

Dominance interactions affected patterns of non-reproductive division of labor (polyethism) in the eusocial wasp Mischocyttarus mastigophorus. Socially dominant individuals foraged for food (nectar and insect prey) at lower rates than subordinate individuals. In contrast, dominant wasps performed most of the foraging for the wood pulp used in nest construction. Social dominance also affected partitioning of materials collected by foragers when they returned to the nest. Wood pulp loads were never shared with nest mates, while food loads, especially insect prey, were often partitioned with other wasps. Dominant individuals on the nest were more likely to take food from arriving foragers than subordinate individuals. The role of dominance interactions in regulating polyethism has evolved in the eusocial paper wasps (Polistinae). Both specialization by foragers and task partitioning have increased from basal genera (independent-founding wasps, including Mischo-cyttarus spp.) to more derived genera (swarm-founding Epiponini). Dominance interactions do not regulate forager specialization or task partitioning in epiponines. I hypothesize that these changes in polyethism were enabled by the evolution of increased colony size in the Epiponini. Received: 8 December 1997 / Accepted after revision: 28 March 1998     

Queen primer pheromone affects conspecific fire ant (<Emphasis Type="Italic">Solenopsis invicta</Emphasis>) aggression

Monogyne fire ant, Solenopsis invicta, colony workers are territorial and are aggressive toward members of other fire ant colonies. In contrast, polygyne colony workers are not aggressive toward non-nestmates, presumably due to broader exposure to heritable and environmentally derived nestmate recognition cues (broad template). Workers from both monogyne and polygyne fire ant colonies execute newly mated queens after mating flights. We discovered that monogyne and polygyne queens have a remarkable effect on conspecific recognition. After removal of their colony queen, monogyne worker aggression toward non-nestmate conspecifics quickly drops to merely investigative levels; however, heterospecific recognition/aggression remains high. Queenless monogyne or polygyne worker groups were also not aggressive toward newly mated queens. Queenless worker groups of both forms that adopted a monogyne-derived newly mated queen became aggressive toward non-nestmate workers and newly mated queens. We propose that the powerful effect of fire ant queens on conspecific nestmate recognition is caused by a queen-produced recognition primer pheromone that increases the sensitivity of workers to subtle quantitative differences in nestmate recognition cues. This primer pheromone prevents the adoption of newly mated queens (regulation of reproductive competition) in S. invicta and when absent allows queenless workers to adopt a new queen readily. This extraordinary discovery has broad implications regarding monogyne and polygyne colony and population dynamics.