The role of competition in task switching during colony emigration in the ant Leptothorax albipennis

The decision-making process that determines when an animal should switch between tasks is a fundamental issue in the study of animal behaviour. We investigated, for the first time, such task switching in terms of the dynamics of worker populations in ant colonies. During colony emigration in the ant Leptothorax albipennis, the colony has to carry out the following three tasks: (1) transport of brood and nestmates to the new nest; (2) sorting of the brood into its characteristic pattern; and (3) building the nest wall. At the beginning of the emigration, the stimuli for all three tasks increase simultaneously but the tasks are performed sequentially by populations of workers in the colony. The issue here is how decision making at the colony level is based on the behaviour of individual workers. We used a mathematical model to explore the hypothesis that such colony level task switching is based on tasks competing for workers. The essential feature of this model is that the sequence of tasks performed by an individual worker need not match the sequence of tasks on which the colony concentrates. We base the parameterization of our model on our detailed experimental study of eight emigrations, one for each of eight L. albipennis colonies. We compared our results with earlier work that emphasizes the role of response thresholds in task-related decisions. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Task allocation in ant colonies within variable environments (A study of temporal polyethism: Experimental)

We briefly review the literature on the division of labour in ant colonies with monomorphic worker populations, and show that there are anomalies in current theories and in the interpretation of existing data sets. Most ant colonies are likely to be in unstable situations and therefore we doubt if an age-based division of labour can be sufficiently flexible. We present data for a type of small ant colony in a highly seasonal environment, concentrating on individually marked older workers. We show that contrary to expectation such workers undertake a wide variety of tasks and can even retain their ability to reproduce, even whilst younger workers are actively foraging. Our analysis shows that old workers occupy four distinct spatial stations within the nest and that these are related to the tasks they perform. We suggest that correlations between age and task in many ant colonies might simply be based on ants foraging for work, i.e. actively seeking tasks to perform and remaining faithful to these as long as they are profitably employed. For this reason, employed older workers effectively displace unemployed younger workers into other tasks. In a companion paper, Tofts 1993,Bull. math. Biol. develops an algorithm that shows how foraging for work can be an efficient and flexible mechanism for the division of labour in social insects. The algorithm creates a correlation between age and task purely as a by-product of itsmodus operandi.     

Genetic variation and task specialization in the desert leaf-cutter ant, Acromyrmex versicolor

The genetic diversity in social insect colonies that is generated by multiple mating or multiple queens has been hypothesized to promote worker task specialization and therefore facilitate division of labour. However, few studies have actually examined the mechanisms by which genotype may influence individual worker behaviour. In this study, we dissect possible genetic effects on worker task performance in the desert leaf-cutter ant. We hypothesize that genotype could affect worker behaviour via (1) the rate of age-related task switching (age polyethism schedule), (2) individual task preference, and/or (3) task performance rates. To discriminate among these possible mechanisms, we generated composite colonies of workers from different genetic sources and followed the behaviour of individually marked workers over their lifetimes. We found significant differences among matrilines (offspring of different queens) in overall task performance. In particular, we found a negative covariance in likelihood of foraging versus tending fungus inside the nest. Workers of different matrilines also varied in the age of transition from inside the nest to foraging, but did not vary in task performance rates. Our results suggest that division of labour in this system is affected by genetic influences on individual task preference and age-related task choice, but not on variation in activity level.     

Mechanisms of interspecific competition among an invasive and two native fire ants

The mechanisms of interspecific competition among an invasive and two native Solenopsis fire ant forms were investigated in a series of laboratory experiments. In separate trials each with a different food resource, the native S. geminata × xyloni retrieved the greatest amount of a protein- and lipid-rich artificial food resource and a high protein natural food resource, and the native S. geminata retrieved the greatest amount of a high carbohydrate food resource. In trials investigating aspects of interference competition at the colony level, the invasive S. invicta proved to be initially more aggressive than S. geminata , but less aggressive than S. geminata × xyloni . Solenopsis invicta eventually controlled more of the foraging arenas against both native forms when colonies were equivalent by worker biomass, but not when colonies were equivalent by worker number. When paired with S. invicta , S. geminata suffered a significantly greater proportional reduction in both workers and entire colonies when colonies were initially standardized by worker biomass, but not when colonies were standardized by worker number. When paired with S. invicta , a significantly greater proportional reduction of workers occurred in S. geminata × xyloni , regardless of how colonies were standardized. In pairwise trials at the individual level, majors always exhibited significantly less mortality than minors, regardless of the Solenopsis form. The majors of both native forms suffered significantly less mortality than those of S. invicta . Superiority in colony-level interference ability appears to be an important mechanism allowing S. invicta to displace native Solenopsis forms. The ability of S. invicta to reach high population densities, because of intrinsic biological characteristics or an escape from natural enemies, plays an important contributory role. Similar mechanisms may underlie the success of other invasive ant species.     

Colony fusion and worker reproduction after queen loss in army ants

Theory predicts that altruism is only evolutionarily stable if it is preferentially directed towards relatives, so that any such behaviour towards seemingly unrelated individuals requires scrutiny. Queenless army ant colonies, which have anecdotally been reported to fuse with queenright foreign colonies, are such an enigmatic case. Here we combine experimental queen removal with population genetics and cuticular chemistry analyses to show that colonies of the African army ant Dorylus molestus frequently merge with neighbouring colonies after queen loss. Merging colonies often have no direct co-ancestry, but are on average probably distantly related because of overall population viscosity. The alternative of male production by orphaned workers appears to be so inefficient that residual inclusive fitness of orphaned workers might be maximized by indiscriminately merging with neighbouring colonies to increase their reproductive success. We show that worker chemical recognition profiles remain similar after queen loss, but rapidly change into a mixed colony Gestalt odour after fusion, consistent with indiscriminate acceptance of alien workers that are no longer aggressive. We hypothesize that colony fusion after queen loss might be more widespread, especially in spatially structured populations of social insects where worker reproduction is not profitable.     

Optimization, conflict, and nonoverlapping foraging ranges in ants

An organism's foraging range depends on the behavior of neighbors, the dynamics of resources, and the availability of information. We use a well-studied population of the red harvester ant Pogonomyrmex barbatus to develop and independently parameterize models that include these three factors. The models solve for an allocation of foraging ants in the area around the nest in response to other colonies. We compare formulations that optimize at the colony or individual level and those that do or do not include costs of conflict. Model predictions were compared with data collected on ant time budgets and ant density. The strategy that optimizes at the colony level but neglects costs of conflict predicts unrealistic levels of overlap. In contrast, the strategy that optimizes at the individual level predicts realistic foraging ranges with or without inclusion of conflict costs. Both the individual model and the colony model that includes conflict costs show good quantitative agreement with data. Thus, an optimal foraging response to a combination of exploitation and interference competition can largely explain how individual foraging behavior creates the foraging range of a colony. Deviations between model predictions and data indicate that colonies might allocate a larger than optimal number of foragers to areas near boundaries between foraging ranges.     

Testing the importance of the distribution of worker sizes to colony performance in the ant species <Emphasis Type="Italic">Formica obscuripes</Emphasis> Forel

We examined the relationship between colony performance and the distribution of worker sizes within colonies in the ant species, Formica obscuripes. We manipulated the distribution of worker sizes within colonies and found that experimental colonies whose distributions mimicked the natural distributions retained a larger percentage of colony biomass over three weeks when fed on honeydew, relative to colonies composed of only large or only small workers. In natural colonies most of the variation in worker sizes was found within, as opposed, to between colonies, suggesting that homeostatic mechanisms within colonies regulated the distribution of worker sizes. While there were no disjunctions in the distribution of worker sizes within colonies, the distribution tended to be bimodal. This study demonstrates that the distribution of worker sizes within colonies is important even for ant species that lack discrete worker castes. Received 31 October 2006; revised 26 December 2006; accepted 4 January 2007.     

Task-specific expression of the foraging gene in harvester ants

In social insects, groups of workers perform various tasks such as brood care and foraging. Transitions in workers from one task to another are important in the organization and ecological success of colonies. Regulation of genetic pathways can lead to plasticity in social insect task behaviour. The colony organization of advanced eusocial insects evolved independently in ants, bees, and wasps and it is not known whether the genetic mechanisms that influence behavioural plasticity are conserved across species. Here we show that a gene associated with foraging behaviour is conserved across social insect species, but the expression patterns of this gene are not. We cloned the red harvester ant (Pogonomyrmex barbatus) ortholog (Pbfor) to foraging, one of few genes implicated in social organization, and found that foraging behaviour in harvester ants is associated with the expression of this gene; young (callow) worker brains have significantly higher levels of Pbfor mRNA than foragers. Levels of Pbfor mRNA in other worker task groups vary among harvester ant colonies. However, foragers always have the lowest expression levels compared to other task groups. The association between foraging behaviour and the foraging gene is conserved across social insects but ants and bees have an inverse relationship between foraging expression and behaviour.     

Extraordinary starvation resistance in Temnothorax rugatulus (Hymenoptera, Formicidae) colonies: Demography and adaptive behavior

Summary. Ant colony mortality has not been sufficiently studied, even though it is crucial for understanding social insect population biology and can serve as an important model for general aging and mortality processes. Particularly, studies on proximate mechanisms on mortality and stress resistance of ant colonies are lacking. This study explores the long-term colony starvation resistance of the small myrmecine ant Temnothorax rugatulus. We report extraordinary starvation resistance in the 21 colonies investigated, as most survived the eight months of total starvation. Furthermore, we studied demographic and behavioral changes over the experimental period. Brood decline began first (after two months) and mortality was highest, worker decline was intermediate, and queen mortality started latest and remained lowest. We found brood (its relative change during the first four months and the level of brood relative to colony size) to be the only significant predictor of colony starvation resistance, but not the degree of polygyny. As expected, rates of trophallaxis increased during the starvation period while colony activity bouts occurred more frequently but were much shorter, leading to an overall decrease in activity levels. This study is the first to comprehensively study mechanisms of starvation resistance in ant colonies, linking demography and behavior.Received 10 January 2005; revised 16 February 2005; accepted 23 February 2005.     

Life‐history strategy and behavioral type: risk‐tolerance reflects growth rate and energy allocation in ant colonies

Despite the recent interest in animal personality and behavioral syndromes, there is a paucity of explanations for why distinct behavioral traits should evolve to correlate. We investigate whether such correlations across apparently distinct behavioral traits may be explained by variation in life history strategy among individual ant colonies. Life history theory predicts that the way in which individuals allocate energy towards somatic maintenance or reproduction drives several distinct traits in physiology, morphology, and energy use; it also predicts that an individual's willingness to engage in risky behaviors should depend on reproductive strategy. We use Temnothorax ants, which have been shown to exhibit ‘personalities’ and a syndrome that may reflect risk tolerance at the colony level. We measure colonies' relative investment in growth rate (new workers produced) compared to reproductive effort (males and queens produced). Comparing sterile worker production to reproductive alate production provides a direct measure of how colonies are investing their energy, analogous to investment in growth versus reproduction in a unitary organism. Consistently with this idea, we found that behavioral type of ant colonies was associated with their life history strategy: risk‐tolerant colonies grew faster and invested more in reproduction, whereas risk‐averse colonies had lower growth rate but invested relatively more in workers. This provides evidence that behavioral syndromes can be a consequence of life‐history strategy variation, linking the two fields and supporting the use of an integrative approach.     

Colony-size effects on task organization in the harvester ant Pogonomyrmex californicus

Colony size is a fundamental attribute of insect societies that appears to play an important role in their organization of work. In the harvester ant Pogonomyrmex californicus, division of labor increases with colony size during colony ontogeny and among unmanipulated colonies of the same age. However, the mechanism(s) integrating individual task specialization and colony size is unknown. To test whether the scaling of division of labor is an emergent epiphenomenon, as predicted by self-organizational models of task performance, we manipulated colony size in P. californicus and quantified short-term behavioral responses of individuals and colonies. Variation in colony size failed to elicit a change in division of labor, suggesting that colony-size effects on task specialization are mediated by slower developmental processes and/or correlates of colony size that were missing from our experiment. In contrast, the proportional allocation of workers to tasks shifted with colony size, suggesting that task needs or priorities depend, in part, on colony size alone. Finally, although task allocation was flexible, colony members differed consistently in task performance and spatial tendency across colony size treatments. Sources of interindividual behavioral variability include worker age and genotype (matriline).     

Northward expansion of the invasive Linepithema humile (Hymenoptera: Formicidae) in the eastern United States is constrained by winter soil temperatures

The invasive Argentine ant, Linepithema humile (Mayr) (Hymenoptera: Formicidae) has been evident in the North Carolina Piedmont, United States for 90 yr but has failed to spread further north. We investigated the mechanisms preventing this expansion. The Argentine ant ceases foraging at temperatures below 5°C and we hypothesized that winter soil temperatures at higher latitudes restricted foraging long enough to cause colony starvation. We tested if the Argentine ant could successfully feed at temperatures below 5°C and found that colonies would starve. We subjected Argentine ant nests to a range of sub- and above-freezing temperatures and measured worker mortality at various time intervals. We found that Argentine ant colonies will collapse after 8.5 d at 5°C. Argentine ants can escape ambient cold temperatures by moving nests into the soil column. We tested how deeply into the soil Argentine ant queens and workers need to move to survive winter in North Carolina. Soil temperatures in the North Carolina Piedmont do not fall below 5°C for longer than nine consecutive days; therefore, Argentine ant colonies need only to retreat a few centimeters into the soil column to escape unsuitable temperatures. Winter soil temperature data from four climate stations situated from latitudes 35°, the current Eastern United States latitudinal limit for Argentine ant population expansion, to 39° were searched for periods where soil temperatures would have led to colony extirpation. North of their current distributions, extended periods of soil temperatures below 5°C regularly occur, preventing Argentine ant colonies from persisting.     

Experimental manipulation of queen number affects colony sex ratio investment in the highly polygynous ant Formica exsecta

In polygynous (multiple queens per nest) ants, queen dispersal is often limited with young queens being recruited within the parental colony. This mode of dispersal leads to local resource competition between nestmate queens and is frequently associated with extremely male-biased sex ratios at the population level. The queen-replenishment hypothesis has been recently proposed to explain colony sex ratio investment under such conditions. It predicts that colonies containing many queens (subject to high local resource competition) should only produce males, whereas colonies hosting few queens (reduced or no local resource competition) should produce new queens in addition to males. We experimentally tested this hypothesis in the ant Formica exsecta by manipulating queen number over three consecutive years in 120 colonies of a highly polygynous population. Queens were transferred from 40 colonies into another 40 colonies while queen number was not manipulated in 40 control colonies. Genetic analyses of worker offspring revealed that our treatment significantly changed the number of reproductive queens. The sex ratio of colonies was significantly different between treatments in the third breeding season following the experiment initiation. We found that, as predicted by the queen-replenishment hypothesis, queen removal resulted in a significant increase in the proportion of colonies that produced new queens. These results provide the first experimental evidence for the queen-replenishment hypothesis, which might account for sex ratio specialization in many highly polygynous ant species.     

Chemical basis of nest-mate discrimination in the ant Formica exsecta.

Distinguishing nest-mates from non-nest-mates underlies key animal behaviours, such as territoriality, altruism and the evolution of sociality. Despite its importance, there is very little empirical support for such a mechanism in nature. Here we provide data that the nest-mate recognition mechanism in an ant is based on a colony-specific Z9-alkene signature, proving that surface chemicals are indeed used in ant nest-mate recognition as was suggested 100 years ago. We investigated the cuticular hydrocarbon profiles of 10 Formica exsecta colonies that are composed almost entirely of a Z9-alkene and alkane component. Then we showed that worker aggression is only elicited by the Z9-alkene part. This was confirmed using synthetic Z9-alkene and alkane blends matched to the individual colony profiles of the two most different chemical colonies. In both colonies, only glass beads with 'nest-mate' alkene profiles received reduced aggression. Finally, changing the abundance of a single Z9-alkene on live ants was shown to significantly increase the aggression they received from nest-mates in all five colonies tested. Our data suggest that nest-mate discrimination in the social insects has evolved to rely upon highly sensitive responses to relatively few compounds.     

Unexpected benefit of a social parasite for a key fitness component of its ant host

Numerous invertebrates inhabit social insect colonies, including the hoverfly genus Microdon, whose larvae typically live as brood predators. Formica lemani ant colonies apparently endure Microdon mutabilis infections over several years, despite losing a considerable fraction of young, and may even produce more gynes. We present a model for resource allocation within polygynous ant colonies, which assumes that whether an ant larva switches development into a worker or a gyne depends on the quantity of food received randomly from workers. Accordingly, Microdon predation promotes gyne development by increasing resource availability for surviving broods. Several model predictions are supported by empirical data. (i) Uninfected colonies seldom produce gynes. (ii) Infected colonies experience a short-lived peak in gyne production leading to a bimodal distribution in gyne production. (iii) Low brood : worker ratio is the critical mechanism controlling gyne production. (iv) Brood : worker ratio reduction must be substantial for increased gyne production to become noticeable.     

Variation in patriline reproductive success during queen production in orphaned colonies of the thelytokous ant Cataglyphis cursor

In genetically diverse insect societies (polygynous or polyandrous queens), the production of new queens can set the ground for competition among lineages. This competition can be very intense when workers can reproduce using thelytoky as worker lineages that manage to produce new queens gain a huge benefit. Selection at the individual level might then lead to the evolution of cheating genotypes, i.e. genotypes that reproduce more than their fair share. We studied the variation in reproductive success among worker patrilines in the thelytokous and highly polyandrous ant Cataglyphis cursor. Workers produce new queens by thelytoky in orphaned colonies. The reproductive success of each patriline was assessed in 13 orphaned colonies using genetic analysis of 433 workers and 326 worker-produced queens. Our results show that patrilines contributed unequally to queen production in half of the colonies, and the success of patrilines was function of their frequencies in workers. However, over all colonies, we observed a significant difference in the distribution of patrilines between workers and worker-produced queens, and this difference was significant in three of 13 colonies. In addition, six colonies contained a low percentage of foreign workers (drifters), and in one colony, they produced a disproportionably high number of queens. Hence, we found some evidence for the occurrence of rare cheating genotypes. Nevertheless, cheating appears to be less pronounced than in the Cape Honey bee, a species with a similar reproductive system. We argue that worker reproduction by parthenogenesis might not be common in natural populations of C. cursor.     

Genetic effects on task performance,but not on age polyethism,in a swarm-founding eusocial wasp

Division of labour among workers in insect societies often includes two major components: age-related changes in behaviour (age polyethism) and specialization in task performance. The aim of this study was to test whether similarity in inside-nest task performance and in rate of age polyethism correspond to genetic similarity among nestmates in the polygynous eusocial waspPolybia aequatorialis.Behavioural data were collected on marked, known-age workers from three source colonies introduced into two observation colonies in the field. Genetic similarity among workers was assessed by quantifying sharing of random amplified polymorphic DNA (RAPD) marker alleles. Workers were categorized by whether they engaged in nest cleaning as an indicator of individual differences in inside-nest task performance. Within source colonies, workers that performed nest-cleaning tasks were more genetically similar to each other than they were to workers not performing these tasks. Workers also differed in their rates of passage through the age-related task sequence, but no association was found between sharing of RAPD marker alleles and rate of age polyethism. These results accord with earlier studies demonstrating flexibility in age polyethism in swarm-founding wasps, and with findings that worker genotypic variability corresponds to specialization in task performance inP. aequatorialis. Polybiaspp. workers rarely switch among tasks, even in response to changes in colony conditions, and workers’ genotypes may constrain flexibility in task performance at the individual level. Conversely, colonies may accrue benefits from having genotypically diverse worker forces, which could favour the maintenance of polygyny in swarm-founding wasps.     

Effects of colony-level attributes on larval feeding in the fire ant, Solenopsis invicta

Summary: Do colony attributes modulate individual behavior? The effects of colony size and worker:brood ratio on the rate of worker-to-larva trophallaxis in the fire ant, Solenopsis invicta, were investigated. Neither colony size ranging from 100 to 10,000 nor worker:brood ratio ranging from 1:1 to 16:1 affected the density of workers on the brood pile, nor the rate or duration of worker-to-larva trophallaxis. The demands of hungry larvae were met even in groups as small as 100 workers in worker:brood ratios as small as 1. Only when the worker:brood ratio was less than 1, were larvae tended or fed at reduced rates. Under natural conditions, this occurs only in incipient colonies. Otherwise, in post-incipient colonies, the flow of food to larvae was unmodified by colony attributes. The implications of this finding are two-fold: First, it reinforces previous research demonstrating that social feeding in the fire ant emerges from localized interactions rather than mass communication. Second, it highlights the resiliency of this weedy species. Hypothetically, colonies drastically reduced by catastrophic events such as flooding should still be able to produce sexuals.     

Reproductive conflicts in polyandrous and polygynous ant Formica sanguinea

The occurrence of multiple reproductives within an ant colony changes the balance between indirect fitness benefits and reproductive competition. We test whether the number of matings by an ant queen (polyandry) correlates negatively with the number of reproductive queens in the colony (polygyny), whether the patrilines and matrilines differ in their contribution to the sexual and worker progeny and whether there is an overall reproductive skew. For these aims, we genotyped both worker and sexual offspring from colonies of the ant Formica sanguinea in three populations. Most colonies were monogynous, but eight (11%) were polygynous with closely related queens. Most queens in the monogynous colonies (86%) had mated with multiple males. The effective paternity was lower than the actual number of mates, and the paternity skew was significant. Furthermore, in some monogynous colonies, the patrilines were differently represented in the worker pupae and sexual pupae produced at the same time. Likewise, the matrilines in polygynous colonies were differently present in worker pupae and male offspring. The effective number of matings by a queen was significantly lower in polygynous colonies (mean m_e = 1.68) than in monogynous colonies (means 2.06–2.61). The results give support to the hypotheses that polyandry and polygyny are alternative breeding strategies and that reproductive competition can lead to different representation of patrilines and matrilines among the sexual and worker broods.     

Influence of toxic bait type and starvation on worker and queen mortality in laboratory colonies of Argentine ant (Hymenoptera: Formicidae)

The efficacy of toxic baits should be judged by their ability to kill entire ant colonies, including the colony queen or queens. We studied the efficacy of four toxic baits to the Argentine ant, Linepithema humile (Mayr) (Hymenoptera: Formicidae). These baits were Xstinguish that has the toxicant fipronil, Exterm-an-Ant that contains both boric acid and sodium borate, and Advion ant gel and Advion ant bait arena that both have indoxacarb. Experimental nests contained 300 workers and 10 queen ants that were starved for either 24 or 48 h before toxic bait exposure. The efficacy of the toxic baits was strongly influenced by starvation. In no treatment with 24-h starvation did we observe 100% worker death. After 24-h starvation three of the baits did not result in any queen deaths, with only Exterm-an-Ant producing an average of 25% mortality. In contrast, 100% queen and worker mortality was observed in colonies starved for 48 h and given Xstinguish or Exterm-an-Ant. The baits Advion ant gel and Advion ant bait arena were not effective against Argentine ants in these trials, resulting in <60% mortality in all treatments. Because of the strong influence of starvation on bait uptake, control efficacy may be maximized by applying bait when ants are likely to be starved. Our results suggest queen mortality must be assessed in tests for toxic bait efficacy. Our data indicate that of these four baits, Xstinguish and Exterm-an-Ant are the best options for control of Argentine ants in New Zealand.