Tool use by the forest ant Aphaenogaster rudis: Ecology and task allocation

Debris dropping behavior by ants during foraging has been labeled alternately as tool use or a protective behavior. To address this controversy, we investigated the circumstances under which the common forest ant Aphaenogaster rudis drops and retrieves debris in the forests of Vermont, in the U.S.A. We tested the hypotheses, first, that debris dropping functions to protect workers from entanglement or drowning in liquids, and second, that debris dropping functions as part of foraging tool use. To determine how workers are allocated to the debris dropping and retrieval tasks, we studied individually marked foragers in the field and laboratory. Our results provide evidence that the debris dropping behavior of Aphaenogaster rudis deserves to be labeled as foraging tool use; A. rudis ants do not drop debris in non-food substances that present a hazard of entanglement or drowning to workers. We also found that potential tools represent a small, but non-negligible, percentage of the items that A. rudis foragers bring back to their colonies. Furthermore, debris dropping by A. rudis at baits discouraged colonization by other ant species. Finally, we provide the first evidence that tool use is a specialized task performed by a subset of A. rudis foragers within each colony at any given point in time. The execution of this task by a small proportion of workers may enhance the competitive ability of this ecologically dominant forest ant. Received 3 April 2006; revised 13 August 2006; accepted 1 September 2006.     

Foraging patterns in three sympatric forest ant species, Prenolepis imparis, Paratrechina melanderi and Aphaenogaster rudis (Hymenoptera: Formicidae)

Abstract.

• 1 Ecological segregation was studied in Aphaenogaster rudis Emery, Paratrechina melanderi (Wheeler) and Prenolepis imparis (Say), the three commonest surface-foraging ants in a Maryland (U.S.A.) hardwood forest community.
• 2 P.imparis retreats from the surface during mid-summer, but shows more cool-season activity than do the other two species. P.melanderi is most active during the warmest months of the years. A.rudis is the most generalized of the three species in its seasonal activity pattern.
• 3 P.imparis is a highly aggressive species which forms large mobilizations at rich food sources. P.melanderi is a timid species which forms small mobilizations. A.rudis is intermediate in both respects.
• 4 Based on the results of baiting trials, P.imparis shows an apparent preference for protein-fat food, P.melanderi prefers carbohydrate food, and A.rudis exhibits no significant preference for either fclod type.
• 5 As a result of its extended seasonal activity, weak circadian periodicity, and lack of food specialization, A.rudis has the broadest annual niche of the three species studied.
• 6 The unusual seasonal activity pattern of P.imparis results in a relatively low degree of annual niche overlap between this species and either of the other two. Overlap between A.rudis and P.melanderi is substantially higher.
• 7 Experimental manipulations confirm that rates of resource removal by a behaviourally subordinate species (Amdis) are reduced in the presence of a dominant species (P.imparis).
• 8 Persistence of these three widespread, abundant, relatively generalized ant species in local sympatry may in part reflect their differential success in: (a) finding food, (b) defending food, and (c) handling food items of different sizes.

     

Queen recruitment and split sex ratios in polygynous colonies of the ant Formica exsecta

Sex ratios in social insects have become a general model for tests of inclusive fitness theory, sex ratio theory and parent–offspring conflict. In populations of Formica exsecta with multiple queens per colony , sex ratios vary greatly among colonies and the dry-weight sex ratio is extremely male-biased, with 89% of the colonies producing males but no gynes (reproductive females). Here we test the queen-replenishment hypothesis, which was proposed to explain sex ratio specialization in this and other highly polygynous ants (i.e. those with many queens per nest). This hypothesis proposes that, in such ants, colonies produce gynes to recruit them back into the colony when the number of resident queens falls below a given threshold limiting colony productivity or survival. We tested predictions of the queen-replenishment hypothesis by following F. exsecta colonies across two breeding seasons and relating the change in effective queen number with changes in sex ratio, colony size and brood production. As predicted by the queen-replenishment hypothesis, we found that colonies that specialized in producing females increased their effective queen number and were significantly more likely to specialize in male production the following year. The switch to male production also coincided with a drop in productivity per queen as predicted. However, adoption of new queens did not result in a significant increase in total colony productivity the following year. We suggest that this is because queen production comes at the expense of worker production and thus queen production leads to resource limitation the following year, buffering the effect of greater queen number on total productivity.     

Dynamics of colony emigration in the ant Aphaenogaster senilis

In many social insect species, colonies frequently emigrate to a new nest. This requires the coordination of many individuals, and it puts the queen at risks of being lost or predated. We experimentally studied colony emigration in the ant Aphaenogaster senilis, who emigrates frequently and obligatorily reproduces by colony fission. As in other species, colony emigration was characterised by a synchronised relocation of workers. Foragers found the new nest site and triggered the relocation of the “inside” workers, which built up following a sigmoid curve. Unlike in Temnothorax, where workers are transported to the new nest, most individuals relocated by walking. The brood was transported around the middle of colony relocation, mostly by “inside” workers because they represent most of the workforce. The queen walked to the new nest at the middle of colony relocation, when the flow of ants to the new nest was maximal. Overall, this temporal dynamic of colony emigration is similar to that observed in other species. However, we argue that species-specific traits, such as whether workers are transported to the new nest or relocate by themselves, may affect parts of the process of colony emigration.     

Resources and the flexible allocation of work in the desert ant, Aphaenogaster cockerelli

Summary: Social insect colonies can respond to changes in resource availability by altering their foraging behavior. Colonies of the desert ant, Aphaenogaster cockerelli, responded to experimental changes in the distribution and type of available resources by adjusting the numbers of ants engaged in foraging and other tasks outside the nest, and by adjusting the temporal patterns of these activities. Colonies foraged more intensely for protein resources than for seed resources, and for high-density resources more than for low-density resources. This flexible allocation and resource use may promote coexistence with interspecific competitors such as ants in the genus Myrmecocystus.     

Sex investment ratios in monogyne and polygyne populations of the fire ant Solenopsis invicta

Both monogyne (single queen per colony) and polygyne (multiple queens per colony) populations of the fire ant Solenopsis invicta are good subjects for tests of kin selection theory because their genetic and reproductive attributes are well-characterized, permitting quantitative predictions about the degree to which sex investment ratios should be female-biased if workers and not queens control reproductive allocation. In the study populations, an investment ratio of 3 females: 1 male is predicted (a proportional investment in females of 0.75) in the monogyne form, whereas a proportional investment in females between 0.637 and 0.740 is expected in the polygyne form. To test these predictions, colonies from a single population of each social form were collected and censused during three different seasons. Consistent with their alternative modes of colony founding, monogyne colonies invested more in reproduction (sexual production) and less in growth/maintenance (worker production) than did the polygyne colonies. Overall, the sex investment ratios were female-biased in both forms, although there was considerable seasonal variation. After adjusting for sex-specific energetic costs, the proportional investment in females was 0.607 in the monogyne population, a value in between those expected under complete control by either the queen or the workers. However, when combined with data from four other previously studied monogyne populations in the U.S.A., the mean investment ratio did not differ significantly from the value predicted if workers have exclusive control. In the polygyne population, the proportional investment in females of 0.616 was consistent with the level of female bias expected under partial to complete worker control, although the potential influence of two confounding factors — possible contact with monogyne colonies and the preponderance of sterile diploid males — weakens this conclusion somewhat. Taken as a whole, the sex investment ratios of monogyne and polygyne populations of S. invicta are consistent with at least partial worker control. Of several ultimate and proximate explanations that have been proposed to explain inter-colonial variation in the sex investment ratio, only the effect of the primary sex ratio (female-determined eggs: male-determined eggs) laid by the queen appears to account for the observed variation among monogyne colonies. In the polygyne population, there is limited support for the hypothesis that greater resource abundance favors investment in females.     

Soil of the nest-mound of the seed-dispersing ant,Aphaenogaster longiceps,enhances seedling growth

Although a major benefit of myrmecochory in the Australian environment is believed to be the targeting of seeds to nutrient-enriched ant nests, there is very little direct evidence for this. Here I report that, compared to control soil, soil from nest mounds of Aphaenogaster longiceps enhances the growth of seedling roots and shoots by about 50% in glasshouse trials. This benefit of nutrient-enrichment, however, probably only occurs when seeds are dispersed by ants that construct large, long-lived, nest mounds. This is very often not the case, and there is now increasing evidence that distance dispersal is often the major benefit of myrmecochory in Australia.     

Frequent nest relocation in the ant Aphaenogaster araneoides: resources, competition, and natural enemies

Sessile and vagile organisms differ from one another in some fundamental ways, including methods of resource acquisition and competition. Ant colonies are typically studied as sessile entities, even though a large fraction of ant species frequently relocate their nests in the course of their life history. Little is known about the causes and consequences of nest relocation, but it is likely that the costs and benefits of relocation are driven by nest quality, neighborhood competition, or resource availability. In this paper, we document several cycles of nest relocation in a population of the Central American ant Aphaenogaster araneoides . In our first experiment, we tracked the pattern of relocation, testing whether environmental characteristics and colony demography were associated with relocation behavior. In our second experiment, we manipulated resource availability by adding or subtracting leaf litter, which is known to predict colony growth. We found that colonies relocated their nests once per week on average and colonies often reoccupied nests from which they had once emigrated. Larger colonies relocated more frequently than smaller colonies, and quickly growing colonies utilized a greater number of nests within their home range compared to slowly growing colonies. Relocation events were most likely to occur in periods when vapor pressure deficits were greatest. Nearest neighbor distance and other measures of environmental conditions were not associated with relocation behavior and there was no significant effect of litter removal or supplementation. We found evidence that multiple natural enemies attacked A. araneoides colonies. Based on the demographic correlates of relocation and our rejection of other plausible hypotheses, we propose that nest relocation is driven by the escape from natural enemies.     

Larval memory affects adult nest-mate recognition in the ant Aphaenogaster senilis

Prenatal olfactory learning has been demonstrated in a wide variety of animals, where it affects development and behaviour. Young ants learn the chemical signature of their colony. This cue-learning process allows the formation of a template used for nest-mate recognition in order to distinguish alien individuals from nest-mates, thus ensuring that cooperation is directed towards group members and aliens are kept outside the colony. To date, no study has investigated the possible effect of cue learning during early developmental stages on adult nest-mate recognition. Here, we show that odour familiarization during preimaginal life affects recognition abilities of adult Aphaenogaster senilis ants, particularly when the familiarization process occurs during the first larval stages. Ants eclosed from larvae exposed to the odour of an adoptive colony showed reduced aggression towards familiar, adoptive individuals belonging to this colony compared with alien individuals (true unfamiliar), but they remained non-aggressive towards adult individuals of their natal colony. Moreover, we found that the chemical similarity between the colony of origin and the adoptive colony does not influence the degree of aggression, meaning that the observed effect is likely to be due only to preimaginal learning experience. These results help understanding the developmental processes underlying efficient recognition systems.     

Foraging arena size and structural complexity affect the dynamics of food distribution in ant colonies

Food acquisition by ant colonies is a complex process that starts with acquiring food at the source (i.e., foraging) and culminates with food exchange in or around the nest (i.e., feeding). While ant foraging behavior is relatively well understood, the process of food distribution has received little attention, largely because of the lack of methodology that allows for accurate monitoring of food flow. In this study, we used the odorous house ant, Tapinoma sessile (Say) to investigate the effect of foraging arena size and structural complexity on the rate and the extent of spread of liquid carbohydrate food (sucrose solution) throughout a colony. To track the movement of food, we used protein marking and double-antibody sandwich enzyme-linked immunosorbent assay, DAS-ELISA. Variation in arena size, in conjunction with different colony sizes, allowed us to test the effect of different worker densities on food distribution. Results demonstrate that both arena size and colony size have a significant effect on the spread of the food and the number of workers receiving food decreased as arena size and colony size increased. When colony size was kept constant and arena size increased, the percentage of workers testing positive for the marker decreased, most likely because of fewer trophallactic interactions resulting from lower worker density. When arena size was kept constant and colony size increased, the percentage of workers testing positive decreased. Nonrandom (clustered) worker dispersion and a limited supply of food may have contributed to this result. Overall, results suggest that food distribution is more complete is smaller colonies regardless of the size of the foraging arena and that colony size, rather than worker density, is the primary factor affecting food distribution. The structural complexity of foraging arenas ranged from simple, two-dimensional space (empty arenas) to complex, three-dimensional space (arenas filled with mulch). The structural complexity of foraging arenas had a significant effect on food distribution and the presence of substrate significantly inhibited the spread of food. Structural complexity of foraging arenas and the resulting worker activity patterns might exert considerable influence on socioecological processes in ants and should be considered in laboratory assays.     

The fate of Corydalis cava elaiosomes within an ant colony of Myrmica rubra: elaiosomes are preferentially fed to larvae

Summary. The diaspores of many plant species are adapted to dispersal by ants (myrmecochory). The ants carry the diaspores into their nests where the appendages of the diaspores (elaiosomes) are consumed. Little is known, however, about the fate of diaspores in the colony, i.e., whether elaiosomes are consumed only by the larvae or also by the workers. In this study, the distribution of Corydalis cava (Fumariaceae) elaiosomes was monitored between the larvae and the working caste of laboratory colonies of Myrmica rubra (Formicidae, Myrmicinae). In the first part of the study, ¹⁵N labelled elaiosomes were found to be mainly consumed by larvae. To find out whether elaiosomes are a more attractive food source than an artificial, nutritionally optimized diet for ants (Bhatkar diet), a combined ¹³C and ¹⁵N labelling experiment was conducted. Ants were offered ¹⁵N labelled elaiosomes for two days (pulse labelling), while being continuously fed with ¹³C labelled Bhatkar diet over 19 days. Under the given laboratory conditions, elaiosomes proved to be a far more attractive diet for the larvae than Bhatkar diet, contributing 87 ± 2% of the daily nitrogen and 79 ± 3% of daily carbon incorporation of larvae during the first four days of the experiment. The mean elaiosome incorporation met 73 ± 5% of nitrogen and 63 ± 6% of carbon demand of workers during the first four days of the experiment. Generally, incorporation rates in workers (per dry body mass) were lower both for carbon and nitrogen during the experiment – by a factor of 6.8 for nitrogen and by a factor of 6.2 for carbon compared to larvae. On a colony basis, workers received 39% and larvae 61% of the elaiosome nitrogen. The results indicate that elaiosomes are a major food source for growing larvae and thus support the hypothesis that elaiosomes play an important role in the life cycle of temperate ants.Received 22 December 2003; revised 16 June 2004; accepted 22 June 2004.     

Self-synchronization and task fulfilment in ant colonies

Some authors have hypothesized that the observed self-synchronized activity in ant colonies provides some adaptive advantages, and, in particular, it has been suggested that task realization may benefit from this ordered temporal pattern of behaviour (Robinson, 1992, Ann. Rev. Entomol, 37, 637-702; Hatcher et al., 1992, Naturwissenschaften, 79, 32-34). In this paper, we use a model of self-synchronized activity (the fluid neural network) to suggest that with self-synchronized patterns of activity a task may be fulfiled more effectively than with non-synchronized activity, at the same average level of activity per individual.     

Nest raiding by the invasive Argentine ant on colonies of the harvester ant, Pogonomyrmex subnitidus

Invasive ants often displace native ants, and published studies that focus on these interactions usually emphasize interspecific competition for food resources as a key mechanism responsible for the demise of native ants. Although less well documented, nest raiding by invasive ants may also contribute to the extirpation of native ants. In coastal southern California, for example, invasive Argentine ants (Linepithema humile) commonly raid colonies of the harvester ant, Pogonomyrmex subnitidus. On a seasonal basis the frequency and intensity of raids vary, but raids occur only when abiotic conditions are suitable for both species. In the short term these organized attacks cause harvester ants to cease foraging and to plug their nest entrances. In unstaged, one-on-one interactions between P. subnitidus and L. humile workers, Argentine ants behaved aggressively in over two thirds of all pair-wise interactions, despite the much larger size of P. subnitidus. The short-term introduction of experimental Argentine ant colonies outside of P. subnitidus nest entrances stimulated behaviors similar to those observed in raids: P. subnitidus decreased its foraging activity and increased the number of nest entrance workers (many of which labored to plug their nest entrances). Raids are not likely to be the result of competition for food. As expected, P. subnitidus foraged primarily on plant material (85% of food items obtained from returning foragers), but also collected some dead insects (7% of food items). In buffet-style choice tests in which we offered Argentine ants food items obtained from P. subnitidus, L. humile only showed interest in dead insects. In other feeding trials L. humile consistently moved harvester ant brood into their nests (where they were presumably consumed) but showed little interest in freshly dead workers. The raiding behavior described here obscures the distinction between interspecific competition and predation, and may well play an important role in the displacement of native ants, especially those that are ecologically dissimilar to L. humile with respect to diet. Received 15 July 2005; revised 19 October 2005; accepted 26 October 2005.     

Coupled oscillators and activity waves in ant colonies

We investigated the phenomenon of activity cycles in ants, taking into account the spatial structure of colonies. In our study species, Leptothorax acervorum, there are two spatially segregated groups in the nest. We developed a model that considers the two groups as coupled oscillators which can produce synchronized activity. By investigating the effects of noise on the model system we predicted how the return of foragers affects activity cycles in ant colonies. We tested these predictions empirically by comparing the activity of colonies under two conditions: when foragers are and are not allowed to return to the nest. The activity of the whole colony and of each group within the colony was studied using image analysis. This allowed us to reveal the spatial pattern of activity wave propagation in ant colonies for the first time.     

Frequent colony relocations do not result in effective dispersal in the gypsy ant Aphaenogaster senilis

Dispersal is an important step in animal's life cycle, one consequence of which is reducing local mate and resource competition. Dispersal is often achieved during one unique special movement, from the birthplace to a new appropriate area where to settle and reproduce. However, in species in which this special movement is limited by life history tradeoffs, we may expect dispersal to be promoted also by routine movements occurring throughout the animal’s life and stimulated by other activities like foraging or the search of nesting conditions. Here we employ a multidisciplinary approach consisting of computer simulations, mark–recapture and genetic data to better understand the role of colony relocations as dispersal strategy in the gypsy ant Aphaenogaster senilis. Contrary to expectations, our results show that colony relocations do not result in effective dispersal as evidenced by mark–recapture and genetic data. Furthermore, simulations showed that successive colony relocations did not follow a constant direction, but occurred either in a randomly changing direction or followed a circular trajectory, indicating limited effective dispersal. We also found a general lack of inbreeding and significant population viscosity between neighbouring colonies suggesting that relocations may act as a balancing strategy between these two processes. We discuss the results in terms of their evolutionary and ecological significance, and highlight future directions of research towards the understanding of dispersal strategies in colonial species.