Trunk trails and the searching strategy of a leaf-cutter ant,Atta colombica

Summary Atta colombica uses chemical mass recruitment that allows the rapid exploitation of resources. Most foragers thus search only within patches. Accumulation of extra foragers at patches results in sampling of alternate food items and area-restricted search as patch resources are depleted.Individual workers have a higher probability of removing a leaf fragment the earlier they arrive at a bait. Workers that arrive when much of the resource is gone travel further on the bait (within the patch) but do not spend significantly more time at the patch. They give up after 50–80s.Foraging effort is centered on the extensive trail system, not on the nest a predicted by time and energy foraging models. Search effort is also trail centered. The probability that an item will be discovered decreases with distance from the trail and increasing litter depth. Trail traffic and trail quality together mave no significant effect although this may be because they act antagonistically.Economic considerations predict that trials should be built to high quality and very productive sites. If trails are built as a result of recruitment and recruitment reflects patch quality and productivity, characteristics of forage sites are physically embodied in the trail system.Leaf cutter foraging is better understood as a long term optimization that effectively exploits resources over the lifetime of the colony than as prudent predation that husbands resources.     

Costs of trail construction and maintenance in the leaf-cutting ant Atta columbica

Leaf-cutting ants of the genus Atta use trunk trails during foraging which may persist for months or years. The time and energy costs of trail construction and maintenance were estimated for colonies of Atta columbica on Barro Colorado Island, Panama, to determine if these costs are likely to constrain new trail construction and promote persistence of existing trails. Large workers 2.2-2.9 mm in headwidth participated in trail-clearing significantly more frequently than typical leaf-carriers, indicating that they may form a distinctive task group within the foraging force. Small litter items were carried off trails, while large ones were cut up before removal, greatly increasing the costs of removing large litter items. The average time cost of removing a kilogram of litter was estimated at 3,359 ant-hours, and energy costs at 4.6 kJ. Colonies maintained trail systems 267 m in length and 16.5 m² in area, and built an estimated 2.7 km of trail with an area of 134 m² during a year. Based on litter standing crop and estimates of litterfall rates, total costs to colonies averaged 11,000 ant-days of work and the energy equivalent of 8,000 leaf burdens. These costs are small relative to the number of available workers and rates of mass harvest, suggesting that costs do not significantly constrain trail construction. Instead, trails may persist because they provide access to high-quality resources or because only a few trails are required to fully exploit the foraging territory.     

Seminal fluid enhances sperm viability in the leafcutter ant Atta colombica

The seminal fluid that accompanies sperm in ejaculates has been shown or suggested to affect sperm competition and paternity success of insects by preventing female remating, inducing oviposition, and forming mating plugs. In Atta leafcutter ants, queens have multiple mates but never remate later in life, although they may live and produce fertilized eggs for several decades. The mating biology and life history of these ants therefore suggests that the major function of seminal fluid is to maximize sperm viability during copulation, sperm transfer, and initial sperm storage. We tested this hypothesis by comparing the viability of testis sperm and ejaculated sperm (mixed with seminal fluid) and found a significant positive effect of seminal fluid on sperm viability. We further quantified this positive effect by adding accessory gland secretion (a major component of seminal fluid) in a dilution series, to show that minute quantities of accessory gland secretion achieve significant increases in sperm viability. Sperm stored by queens for 1 year benefited in a similar way from being exposed to accessory gland compounds after dissection in control saline solution. Our results provide the first empirical evidence that seminal fluid is important for the production of viable ejaculates and that the accessory glands of Atta males—despite their small size—are functional and produce a very potent secretion.     

Multiple mating increases the sperm stores of Atta colombica leafcutter ant queens

Multiple mating is likely to be costly for ant queens and yet it is common. Whether multiple mating brings benefits to queens that outweigh the costs has, therefore, received considerable theoretical attention. Empirical tests of hypotheses have been scarce and no clear evidence has been reported. We tested the “multiple-mating-for-more-sperm” hypothesis on individual young queens in a natural population of the leafcutter ant Atta colombica, a monogynous ant characterised by very large colonies and high colony longevity. We found that the number of sperm stored by queens was positively correlated with the number of mates per queen estimated through mother-offspring analysis with microsatellite DNA markers. Queen sperm stores increased on average by 30 million sperm for each additional mate. Life-history information for Atta indicate that the number of stored sperm observed is likely to constrain the reproductive lifespan of queens in nature. Multiple mating, despite costs, may therefore enhance the fitness of Atta queens because it enables them to store more sperm. Received: 19 September 1997 / Accepted after revision: 7 December 1997     

Task partitioning, division of labour and nest compartmentalisation collectively isolate hazardous waste in the leafcutting ant Atta cephalotes

We studied the organisation of garbage disposal and management in the leafcutting ant Atta cephalotes. The nest of this species has an internal garbage heap to which waste from the fungus garden is taken. The transport of waste from the fungus gardens to the garbage heaps is an example of task partitioning. Ninety-four percent of the garbage loads transferred from the fungus garden to the garbage heap were transferred indirectly via a caching site just outside the garbage heap entrance. A further 3% were transferred directly from a fungus garden worker to a garbage heap worker, again just outside the heap entrance. Only 3% were taken directly to the garbage heap without task partitioning. This is the first described example of task partitioning in insect societies for work other than foraging and the first example of task partitioning occurring entirely within the nest. Furthermore, there is a strong division of labour between the fungus garden workers and the garbage heap workers, with garbage workers hardly ever leaving the heap. Division of labour is reinforced by aggressive behaviour directed towards workers contaminated with garbage. This pattern of work organisation minimises contact between garbage heap workers, who are probably contaminated with pathogens hazardous to both the ants and their symbiotic fungus, and both fungus garden workers and the fungus garden. Task partitioning, division of labour (reinforced by aggression) and nest compartmentalisation act synergistically to isolate the hazardous garbage heap from the fungus gardens.     

Construction of chimaeric gardens through fungal intercropping: a symbiont choice experiment in the leafcutter ant Atta texana (Attini, Formicidae)

Interspecies or intraspecies cooperation can be stabilized evolutionarily if choosing partners favor beneficial partners and discriminate against non-beneficial partners. We quantified such partner choice (symbiont choice) in the leafcutter ant Atta texana (Attini, Formicidae) by presenting the ants in a cafeteria-style preference assay with genotypically distinct fungal cultivars from A. texana and Acromyrmex versicolor. Symbiont choice was measured as the ants' tendency to choose one or more cultivar(s) from several pure (axenic) cultivar fragments and convert a given fungal fragment into a garden. Microsatellite DNA fingerprinting enabled us to identify the cultivars chosen by the ants for their gardens. In 91% of the choice tests, A. texana workers combined multiple cultivars into a single intercropped, chimaeric garden, and the cultivars coexisted in such chimaeric gardens for as long as 4 months. Coexistence of distinct fungal genotypes in chimaeric gardens appears to contradict a recent model of cultivar competition postulating that each cultivar secretes incompatibility compounds harming other cultivars, which presumably would preclude the intercropped polyculture observed in our experiments. Although we found no clear evidence of novel, recombinant genotypes in the experimental chimaeric gardens, the intercropping of cultivar genotypes may occasionally lead under natural conditions to exchange of genetic material between coexisting cultivars, thus introducing novel cultivar genotypes into the leafcutter symbiosis. Symbiont choice by ants and any competition between coexisting cultivar strains in chimaeric gardens do not appear to operate fast enough in our laboratory assay to convert chimaeric gardens into the monocultures observed for A. texana under natural conditions.     

Sociogenetic responses to ecological variation in the ant Myrmica punctiventris are context dependent

Models of social evolution predict a strong relationship between ecological factors and sociogenetic organization in social insects (e.g. queen number, nestmate relatedness and population structure). Despite a large body of coherent theory, empirical support for these predictions is weak. Here we report the results of an experiment that manipulated two ecological parameters, food and nestsite availability, thought to be important for a population of the forest ant Myrmica punctiventris. Earlier work had shown that the sociogenetic structure varies between two populations of this species, and an ecological experiment in one of the populations (in Vermont) revealed that food supplementation had the strongest effects on nestmate relatedness. We repeated the experiment in the second population (in New York) and obtained strikingly different results. We show that nestsite supplementation had the strongest effect in the New York population, and that adding both food and nestsites affected nestmate relatedness in a direction opposite to that reported from the Vermont study. These results show that the ecological context is critically important for understanding the determinants of colony structure in ants. Furthermore, comparison of our data with that of a previous study shows that social organization in New York is temporally unstable. Thus, not only do ecological factors strongly influence social organization, but their influence can vary over time. Our study underscores the need for detailed information on the natural history and ecology of social species.     

Parasitic flies (Diptera: Phoridae) influence foraging rhythms and caste division of labor in the leaf-cutter ant,Atta cephalotes (Hymenoptera: Formicidae)

Summary Three lines of evidence, including interspecific comparisons, temporal division of foraging between size castes, and experimental manipulations, suggest that the diurnal parasitoid Neodohrniphora curvinervis (Diptera: Phoridae) influences both the caste sizes and numbers of leaf-cutter ants (Atta cephalotes) that leave their underground nests to collect leaves. At Parque Nacional Corcovado in Costa Rica, A. cephalotes was attacked by Neodohrniphora during the daytime, and foraged less during the day than at night; a closely related ant at the same site, A. colombica, had no phorid parasites and foraged exclusively during the day. Most daytime foragers of A. cephalotes were smaller than the lower size threshold for attack by Neodohrniphora, while nocturnal foragers, active when parasitoids were absent, were both larger than this threshold and within the energetically optimal size range for foraging. When I supplied artificial lighting to allow phorids to hunt at A. cephalotes colonies past dusk, ants foraged less than when light was provided but flies were removed. The influence of Neodohrniphora on the foraging activity of A. cephalotes may explain why investigations focusing on abiotic factors have largely failed to discover what drives this ant's daily foraging cycles, and suggests that forager sizes are influenced not only by energetic efficiency, but also by the threat of parasitism.     

Allometry and the geometry of leaf-cutting in Atta cephalotes

Summary This study considers the relationship of both leg length and the geometry of leaf-cutting to load-size determination by the highly polymorphic leaf-cutting ant Atta cephalotes. A. cephalotes workers anchor on the leaf edge by their hind legs and pivot around them while cutting arcs from leaves. I tested the hypothesis that, for an ant cutting a semicircular leaf fragment, fragment area is determined by a fixed reach while cutting. This reach hypothesis predicts that ants should cut the same fragment-area for at all leaf types. Also, if the radius of the semicircular fragment is proportional to hind leg length, this hypothesis predicts that leaf area should be proportional to hind-leg length squared. The field work was carried out in March–April 1990 and June 1991 in Heredia Province, Costa Rica. I measured hind-leg length for workers of different masses. I then measured leaf-fragment area and mass for workers cutting semicircular fragments from leaves of different densities (mass/area). The logarithmic relationship between ant mass (M _a) and hind-leg length L accelerated negatively (Fig. 1). As a result of this complex allometry, relative leg length (L/M _a ^0.33) increased with ant mass up to a mass of 7.4 mg. Above 7.4 mg, relative leg length decreased. For foragers cutting semicircular fragments, the area cut by an ant of a given size showed no significant difference among leaves of different densities (Fig. 2). Leaf area (A) increased as a function of leg length to the 1.9 power (Fig. 4), an exponent not significantly different from the square function expected if the radius of a fragment is determined by the ant's reach. As a result of this consistent mode of fragment-area determination, the mass of fragments cut by an ant of a given size was significantly greater when cutting denser leaves (Fig. 3) and relative area (A/M _a) cut decreased with increasing ant mass. However, because larger ants generally cut denser leaves (Table 1), the increased density of thick leaves was offset by the reduced relative area cut by the larger ants. Overall, 93% of the foragers cut fragments weighing between 1.5 and 6 times their own body mass (Table 1). Earlier studies found that this broad load-mass range maximized the biomass-transport rate (mass/distance/time) and transport efficiency (mass/distance/energy cost). Thus, A. cephalotes does not solve the problem of matching ant mass and load mass at leaves of different densities with flexibility in the leaf-cutting behavior of individual ants. Instead, individual ants employ a single simple behavioral rule, but workers of different sizes and body proportions tend to cut leaves of different densities.     

Nestmate recognition and the ontogeny of acceptability in the ant,Leptothorax curvispinosus

Summary In social insects, there is often a brief period following eclosion when workers are highly acceptable in alien nests of their own or other species. This study tested for such an acceptance period in the facultatively polygynous ant, Leptothorax curvispinosus, and compared the duration and effectiveness of this period for conspecific and heterospecific introductions. Workers that eclosed and aged for 1–70 h or 30 days in isolation were introduced into either their parental nests (n=24), alien conspecific nests (n=265), or nests of the closely related and biologically similar species, L. longispinosus (n=341). In alien conspecific nests, acceptance was maximal for workers aged 1–12 h at introduction (67.7% not attacked, 75.8% adopted) and gradually decreased until the level of nonaggression (after 60 h) and adoption (after 36 h) were not significantly different from 30-day-old workers (5.9% not attacked, 17.6% adopted). In heterospecific nests, acceptance was maximal for workers aged 1–4 h at introduction (34.8% not attacked, 37.0% adopted) but thereafter was not significantly different from 30-day-old workers (5.6% not attacked, 8.3% adopted). In their parental nests, workers were generally accepted regardless of age (4–56 h posteclosion, 95.8% not attacked, 100% adopted); a result that is consistent with previous research on older workers (38–157 days posteclosion). This study demonstrates an acceptance period that is more effective and of longer duration within than between these species but that, under uniform laboratory conditions, is often not necessary for the integration of workers into their parental colonies. Within colonies, acceptance periods might only be important during relatively brief periods in a colony's life history when eclosing workers produce genetically based nestmate recongition cues that are not already represented in the colony and must be learned by colony members (e.g., during early colony growth or following adoption of queens), or when young workers must acquire environmentally based nestmate recognition cues to achieve and maintain acceptability.     

Brood-care experience, nursing performance, and neural development in the ant Pheidole dentata

Social insect workers mature behaviorally and physiologically with increasing age, generally transitioning from or adding new tasks to their existing repertoire of within-nest nursing tasks. As adult minor workers of the ant Pheidole dentata age, they attend to brood more frequently and nurse more efficiently, perform a broader array of tasks, and undergo myological and neural development. Because these factors covary, the causal relationships among age, task experience, and neural and physiological maturation are not understood. We compared brood-care performance and efficiency by 10-day-old P. dentata minors that had acquired nursing experience to that of equal-age minors experimentally deprived of brood contact. We found the frequency and efficiency of nursing did not significantly differ between experimental and control worker groups, suggesting experience is not required for age-related improvement in nursing efficiency. Workers with and without prior nursing experience did not significantly differ macroscopically in brain anatomy or in brain serotonin content, although workers from the two treatments had slightly, but significantly, different levels of brain dopamine. These results suggest experience with brood is not required for P. dentata minor workers to develop nursing proficiency or undergo a substantial degree of the age-related neural development identifiable by our assessments, which could underscore the ontogeny of brood-care efficiency.     

Predator-specific alarm calls in Campbell's monkeys, Cercopithecus campbelli

One of the most prominent behavioural features of many forest primates are the loud calls given by the adult males. Early observational studies repeatedly postulated that these calls function in intragroup spacing or intergroup avoidance. More recent field experiments with Diana monkeys (Cercopithecus diana) of Taï Forest, Ivory Coast, have clearly shown that loud male calls function as predator alarm calls because calls reliably (1) label different predator classes and (2) convey semantic information about the predator type present. Here, I test the alarm call hypothesis another primate, the Campbell's monkey (C. campbelli). Like Diana monkeys, male Campbell's monkeys produce conspicuous loud calls to crowned hawk eagles (Stephanoaetus coronatus) and leopards (Panthera pardus), two of their main predators. Playback experiments showed that monkeys responded to the predator category represented by the different playback stimuli, regardless of whether they consisted of (1) vocalisations of the actual predators (crowned hawk eagle shrieks or leopard growls), (2) alarm calls to crowned hawk eagles or leopards given by other male Campbell's monkeys or (3) alarm calls to crowned hawk eagles or leopards given by sympatric male Diana monkeys. These experiments provide further evidence that non-human primates have evolved the cognitive capacity to produce and respond to referential labels for external events.     

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.     

Colony growth and the ontogeny of worker polymorphism in the fire ant,Solenopsis invicta

Summary Colony size and worker polymorphism (headwidth) were determined for fire ant colonies ranging from incipient to 12 years of age. Colonies grew approximately logistically, reaching half size between 21/2 and 31/2 yr and reaching their maximum size of about 220000 workers after 4 to 6 yr. Colony size showed strong seasonal variation. There was some evidence that growth rate may vary with food density. Incipient colonies are monomorphic and consist of small workers only, but as colonies grow, production of larger workers causes the size-frequency distributions to become strongly skewed. These skewed distributions were shown to consist of two slightly overlapping normal distributions, a narrow one defined as the minor workers, and a much broader one defined as the major workers. Major workers differ from minor workers in having been subjected to a discrete, additional stimulation of body growth, resulting in a second normal subpopulation. The category of media is seen to be developmentally undefined. The mean headwidth of the workers in both of these subpopulations increased during the first 6 mo. of colony life, until colonies averaged about 4000 workers. Headwidth of minors declined somewhat in colonies older than about 5 yr, but that of majors remained stable. When the first majors appear, their weight averages about twice that of minors. This increases to about 4 times at 6 mo. and remains stable thereafter. The range of weights of majors is up to 20 times that of minors. Growth of the subpopulation of major workers is also logistic, but more rapid than the colony as a whole, causing the proportion of major workers to increase with colony size. In full sized colonies, about 35% of the workers are majors. Total biomass investment in majors increases as long as colonies grow, beginning at about 10% at 2 months and reaching about 70% in mature colonies. This suggests that major workers play an important role in colony success. The total dry biomass of workers peaked at about 106 g, that of majors at about 72 g. These values then fluctuate seasonally in parallel to number of workers. When colony growth ceases, the proportion of majors remains approximately stable. Colony size explained 98% of the variation in the number of major workers.This is paper No. 18 of the Fire Ant Research Team     

Queen fertility, egg marking and colony size in the ant Camponotus floridanus

In ant societies, workers do not usually reproduce but gain indirect fitness benefits from raising related offspring produced by the queen. One of the preconditions of this worker self-restraint is sufficient fertility of the queen. The queen is, therefore, expected to signal her fertility. In Camponotus floridanus, workers can recognize the presence of a highly fertile queen via her eggs, which are marked with the queen's specific hydrocarbon profile. If information on fertility is encoded in the hydrocarbon profile of eggs, we expect workers to be able to differentiate between eggs from highly and weakly fertile queens. We found that workers discriminate between these eggs solely on the basis of their hydrocarbon profiles which differ both qualitatively and quantitatively. This pattern is further supported by the similarity of the egg profiles of workers and weakly fertile queens and the similar treatment of both kinds of eggs. Profiles of queen eggs correspond to the cuticular hydrocarbon profiles of the respective queens. Changes in the cuticular profiles are associated with the size of the colony the queen originates from and her current egg-laying rate. However, partial correlation analysis indicates that only colony size predicts the cuticular profile. Colony size is a buffered indicator of queen fertility as it is a consequence of queen productivity within a certain period of time, whereas daily egg-laying rate varies due to cyclical oviposition. We conclude that surface hydrocarbons of eggs and the cuticular profiles of queens both signal queen fertility, suggesting a major role of fertility signals in the regulation of reproduction in social insects.     

Queen and worker policing in the monogynous and monandrous ant, Diacamma sp.

Policing behavior that prevents workers from laying male eggs was examined in the monogynous and monandrous ponerine ant Diacamma sp. from Japan, in which a singly mated worker called a “gamergate” reproduces as the functional queen in each colony. Since oviposition by virgin workers is rare in the presence of a gamergate, we separated a portion of workers from the gamergates and induced their oviposition experimentally. When orphaned workers had started to oviposit, they were returned to the original colonies, where they continued to lay eggs for a while. The gamergates and other workers interfered with the laying workers by aggressively taking and finally eating the eggs. In total, 60% and 29% of the worker-derived eggs were eaten by gamergates and non-mother workers, respectively. The observed worker-worker interactions were not driven simply by competition to leave own sons, because non-laying non-orphaned workers interfered with worker reproduction. Furthermore, orphaned workers were usually attacked by non-orphaned workers soon after colony reunification. These results indicate that both queen policing by gamergates and worker policing in this species are mechanisms inhibiting worker oviposition. The gamergate contribution to policing was proportionately larger than that of workers, but among virgin workers, the relationship between dominance rank and contribution to policing was not clear. But about 11% of the eggs were not policed and were added to egg piles, especially in large colonies. Worker policing in a monandrous and monogynous eusocial Hymenoptera contrasts to other recent findings, and possible genetic, social, and ecological factors for its evolution in Diacamma sp. are discussed. Received: 16 November 1998 / Received in revised form: 9 February 1999 / Accepted: 21 February 1999