Between-caste aversion as a basis for division of labor in the ant Pheidole pubiventris (Hymenoptera: Formicidae)

Summary When deprived of minor workers under expermental conditions, major workers of the ant Pheidble pubiventris dramatically increase their repertory and rate of activity, and the change is due in good part to the greater attention they pay the brood. When minor workers are reinstated in appropriate numbers, the majors reduce their attention to the immature stages to the ordinary, low levels. Their response consists of the active avoidance of minors while in the vicinity of the immature stages. However, majors do not turn from other majors near the brood as much as they do from the minors, and they do not avoid minors at all while in other parts of the nest. In addition, minors do not avoid either minors or majors anywhere in the nest. The result is a striking division of labor with reference to brood care.     

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.     

Caste and division of labor in leaf-cutter ants (Hymenoptera: Formicidae: Atta)

Summary Leaf cutting was selected for an evaluation of ergonomic efficiency in the fungus-growing ant Atta sexdens because it is performed largely by medias (head width 1.8–2.8 mm), which attend to relatively few other functions and hence are less likely to be evolutionarily compromised by the demands of competing tasks (Fig. 1).Three alternative a priori criteria of evolutionary optimization were envisioned that are consistent with natura selection theory: the reduction of predation by means of defense and evasion during foraging, the minimization of foraging time through skill and running velocity during foraging, and energetic efficiency, which must be evaluated with reference to both the energetic construction costs of new workers and the energetic cost of maintenance of the existing worker force.In order to measure the performance of various size groups within the A. sexdens worker caste in isolation, I devised the pseudomutant technique: in each experiment, groups of foraging workers were thinned out until only individuals of one size class were left outside the nest. Measurements were then made of the rate of attraction, initiative in cutting, and performance of each size group at head-width intervals of 0.4 mm (Figs. 2, 3, and 7). Other needed measurements were made in body weight, oxygen consumption, and running velocity (Figs. 5, 6, and 8).The size-frequency distribution ff leaf cutters in the A. sexdens conforms closely to the optimum predicted by the energetic efficiency criterion for harder forms of vegetation, such as rhododendron leaves. The distribution is optimum with reference to both construction and maintenance costs. The difference between the predicted and actual modal size groups specializing on leaf cutting is 10% or less of the total size range of the sexdens worker caste.A model was next constructed in which attraction and initiative were allowed to evolve genetically to uniform maximum levels. The theoretical maximum efficiency levels obtained by this means were found to reside in the head-width 2.6–2.8 mm size class, or 8% from the actual maximally efficiency class (head width 2.2–2.4 mm). In the activity of leaf cutting, A. sexdens can therefore be said to be not only at an adaptive optimum but also, within at most a relatively narrow margin of error, to have been optimized in the course of evolution.     

Age-related repertoire expansion and division of labor in Pheidole dentata (Hymenoptera: Formicidae): a new perspective on temporal polyethism and behavioral plasticity in ants

The controversy concerning the extent to which the organization of division of labor in social insects is a developmental process or is based on task allocation dynamics that emerge from colony need independent of worker age and endocrine or neural state has yet to be resolved. We present a novel analysis of temporal polyethism in the ant Pheidole dentata, demonstrating that task attendance by minor workers does not shift among spatially associated sets of behaviors that minimally overlap but rather expands with age. Our results show that the number of tasks performed by older minors increases through the addition and retention of behaviors, with up to a sixfold increase in repertoire size from day 1 to day 20 of adult life. We also show that older minors respond to colony needs by performing significantly more brood care as its demand increases, indicating that they can quickly upregulate nursing according to labor requirements. This level of plasticity was absent in younger siblings. The breadth of responsiveness to task-related olfactory stimuli increased with age. In a binary choice test in which young and old minor workers could orient toward odorants from brood or food, older workers responded to both brood and food, whereas young workers responded only to brood. These dissimilar responses to stimuli associated with nursing and foraging indicate age-related differences in sensory ability and provide a physiological basis for the age-related repertoire expansion model. We discuss repertoire expansion in P. dentata in light of behavioral development and caste flexibility in ants.     

Effects of parasites on foraging and defense behavior of a termitophagous ant,Pheidole titanis Wheeler (Hymenoptera: Formicidae)

Summary Pheidole titanis Wheeler, an ant that occurs in desert and deciduous thorn forest in the southwestern United States and western Mexico, is a predator on termites. In the dry season well-coordinated raids against termite foraging parties occur early in the morning or late in the afternoon, whereas in the wet season most raids occur at night. This seasonal shift in the timing of raids is due to the increased activity of a fly (Diptera: Phoridae) that is a specialist parasitoid on P. titanis workers and soldiers. When parasitic flies discover P. titanis nest entrances or raiding columns, workers stop foraging and defend themselves against oviposition attacks. Flies are only active during the day and never interfere with foraging at night. However, P. titanis does not increase the frequency of raids at night and, as a result, colonies collect less food in the wet season compared to the dry season. Presence of parasitic flies also interferes with normal defense behavior of P. titanis against conspecific and heterospecific enemy ants. Dissections of P. titanis workers and soldiers suggest that the parasitism rate by flies is less than 2% and observations indicate that parasitic flies are much rarer than their host workers and soldiers. Nonetheless, these parasites exert a strong ecological impact on their host.     

Dominance orders in the ponerine ant Pachycondyla apicalis (Hymenoptera,Formicidae)

Summary Intracolony aggression among workers of the neotropical ponerine ant species Pachycondyla apicalis leads to dominance orders. Antagonistic interactions can entail either overt physical attacks with the subordinate individual often exhibiting a submissive posture or the robbing and destruction of eggs laid by nestmates. The single queen, however, was never observed either attacking or being attacked by any colony member. The hierarchical structure among workers consists of one dominant individual and several subordinates; the relationships among subordinate workers are unclear, however. We report for the first time a natural (nonmanipulated) change in the social status of individuals within an ant dominance order. Dominant workers usually had better developed ovaries, laid more eggs and were more frequently observed attending the egg pile than subordinate individuals. This pattern became even more striking when the queen was excluded from the colony. These results indicate that workers of P. apicalis lay eggs even in the presence of the queen. It is possible that some of these haploid eggs may develop into males.Offprint requests to: B. Holldobler     

Queen dimorphism and reproductive strategies in the fire ant Solenopsis geminata (Hymenoptera: Formicidae)

Alate trapping studies of a monogyne population of the fire ant Solenopsis geminata indicate that two sizes of gynes are produced. Macrogynes, which participate in late spring and summer mating flights, are larger, fattier, and more than twice as heavy as microgynes, which participate in fall mating flights. Three patterns of gyne production were observed in 51 colonies studied: 35 produced macrogynes only, 9 produced microgynes only, and 7 produced both morphs, contributing to both summer and fall mating flights. Behavioral evidence and rearing studies suggest that macrogynes found new colonies independently, whereas microgynes achieve colony queen status by infiltrating or being adopted by established colonies. Of the total number of female alates collected from the trapped colonies, 56% were microgynes. However, because of their smaller size and lower fat content, microgynes made up only one-third of the caloric investment in female alates. By measuring the thorax lengths of queens from mature colonies, we determined that at least 56% were macrogynes and 35% or more were microgynes. These results indicate that as a reproductive strategy, colony investment in microgyne production may have at least as high a payoff as investment in macrogyne production.This is publication #24 of the Fire Ant Research Team     

Foraging and spatiotemporal territories in the honey ant Myrmecocystus mimicus wheeler (Hymenoptera: Formicidae)

Summary The honey ant Myrmecocystus mimicus is a scavenger, forages extensively on termites, collects floral nectar, and tends homoptera. Individual foragers of M. mimicus usually disperse in all directions when leaving the nest, but there are also groups of foragers that tend to swarm out of the nest primarily in one direction. Such massive departues are usually at irregular intervals, which may last several hours. The results of field and laboratory experiments suggest that these swarms of foragers are organized by a group recruitment process, during which recruiting scout ants lay chemical orientation trails with hindgut contents and simultaneously stimulate nestmates with a motor display and secretions from the poison gland. Usually these columns travel considerable distances (4–48 m) away from the nest, frequently interfering with the foraging activity of conspecific neighboring colonies.To prevent a neighboring colony from access to temporal food sources or to defend spatiotemporal borders, opposing colonies engage in elaborate display tournaments. Although hundreds of ants are often involved during these tournaments almost no physical fights occur. Instead, individual ants confront each other in highly sterotyped aggressive displays, during which they walk on stilt legs while raising the gaster and head. Some of the ants even seem to inflate their gasters so that the tergites are raised and the whole gaster appears to be larger. In addition, ants involved in tournament activities are on average larger than foragers.The dynamics of the tournament interactions were observed in several colonies over several weeks-mapping each day the locations of the tournaments, the major directions of worker routes away from the nest, and recording the general foraging activities of the colonies. The results indicate that a kind of dominance order can occur among neighboring colonies. On the other hand, often no aggressive interactions among neighboring colonies can be observed, even though the colonies are actively foraging. In those cases the masses of foragers of each colony depart in one major direction that does not bring them into conflict with the masses of foragers of a neighboring colony. This stability, however, can be disturbed by offering a new rich food source to be exploited by two neighboring colonies. This invariably leads to tournament interactions.When a colony is considerably stronger than the other, i.e., with a much larger worker force, the tournaments end quickly and the weaker colony is raided. The foreign workers invade the nest, the queen of the resident colony is killed or dirven off, while the larvae, pupae, callow workers, and honey pot workers are carried or dragged to the nest of the raiders. From these and other observations we conclude that young M. mimicus queens are unlikely to succeed in founding a colony within approximately 3 m of a mature M. mimicus colony because they are discovered and killed, or driven off by workers of the resident colony. Within approximately 3–15 m queens are more likely to start colonies, but these incipient groups run a high risk of being raided and exterminated by the mature colony.Although populations of M. mimicus and M. depilis tend to replace each other, there are areas where both species overlap marginally. Foraging areas and foraging habitats of both species also overlap broadly, but we never observed tournament interactions between M. mimicus and M. depilis.The adaptive significance of the spatiotemporal territories in M. mimicus is discussed.     

Differential reproduction in multiple-queen colonies of the fire ant Solenopsis invicta (Hymenoptera: Formicidae)

Summary The contribution to maternity of workers and female sexuals over time by queens in six multiple-queen laboratory colonies of Solenopsis invicta was directly assessed by use of enzyme genetic markers. Queens contributed more equally to the worker pool than to the pool of sexuals in virtually all samples (Fig. 1), and individuals producing a substantial proportion of the workers often had low or no representation of their daughters in the pool of sexuals. Signficant disparity among queens in their relative production of sexual daughters was often evident, with dominance in production of sexuals by a given queen commonly occurring in association with a pronounced loss of weight followed shortly by her death. The results suggest that significant variability in short-as well as long-term reproductive success may occur among the distantly related queens associating in natural polygyne S. invicta nests. Variance in apportionment of maternity of sexuals did not appear to be simply related to varying levels of fecundity, suggesting that the common presumption that reproductive success can be equated with fecundity in polygyne social Hymenoptera may not be well founded. The observed variance also did not appear to result from a simple mechanism of kin recognition and discrimination by workers in the process of brood rearing. Rather, this variance may have largely resulted from either, 1) recognition of certain queens and their progeny coupled with preferential sexualization of these immatures by nurse workers, or, 2) queen biasing of eggs toward development as sexuals. The frequent association of weight loss and death of mother queens with high levels of sexual daughter production may be best explained by the latter mechanism.     

Colonial recognition of fungus in the fungus-growing ant Acromyrmex subterraneus subterraneus (Hymenoptera: Formicidae)

Summary. Leaf cutting ants live in symbiosis with a basidiomycete fungus that is exploited as a source of nutrients for the ant larvae. Tests of fungus transport demonstrated that Acromyrmex subterraneus subterraneus workers discriminate concolonial fungus from alien fungus, and rejected the latter. Larvae and pupae of the ant were used as controls. Chemical analysis of the fungus revealed a great similarity between its hydrocarbon profile and that found on the ant brood. Experiments with lures showed that chemical extracts from the fungus are responsible for this discrimination process. Moreover, the presence of brood inside the fungus seemed to be important for discrimination of the fungus by workers. Resident workers accepted concolonial broodless fungus less than concolonial fungus inoculated with brood odor. Fungus seems to acquire colonial odor passively, simply by contact with the brood. The impact of fungus volume present in the nest on closure of the colony is discussed. We show here for the first time the importance of a symbiotic vegetal organism in colonial recognition in social insects. Received 14 April 2000; accepted 29 September 2000     

Co-evolution-driven cuticular hydrocarbon variation between the slave-making ant Rossomyrmex minuchae and its host Proformica longiseta (Hymenoptera: Formicidae)

Summary. Proformica longiseta exists as two populations in the Sierra Nevada Mountains in Spain, only one of which is parasitized by the slave-maker ant Rossomyrmex minuchae. To investigate the possible effect of co-evolutionary pressures on cuticular hydrocarbon (CHC) profiles (the presumed nestmate recognition cues), we performed a comparative analysis of the CHC of R. minuchae and P. longiseta colonies from both the allopatric and sympatric populations; the latter includes samples of enslaved as well as free-living workers. Discriminant analyses based on these chemical profiles showed two clear profile groups: the first comprised R. minuchae and both enslaved and free-living P. longiseta from the sympatric population; and the second the allopatric P. longiseta workers. As expected, the profiles of the two sympatric P. longiseta groups (enslaved and free-living) were distinct; but, interestingly, those of the enslaved P. longiseta and its parasite R. minuchae were also distinguishable. This indicates that despite their cohabitation each species maintains its own chemical identity. Profile similarity between the sympatric free-living P. longiseta and its parasite may explain the lower than expected aggression observed during raids. We further speculate that in view of the differences between the sympatric and allopatric population of P. longiseta, co-evolutionary pressures have driven changes in the profile of the former to better match that of its parasite R. minuchae. Such an adjustment may have enabled nests of the sympatric P. longiseta to endure multiple raids by the parasite (due to the reduced aggression) and thus to continue to reproduce despite the damage inflicted by the raids.     

Individually different foraging methods in the desert ant Cataglyphis bicolor (Hymenoptera,Formicidae)

Summary Observations and field experiments on the foraging behaviour of individual workers of Cataglyphis bicolor in a Southern Tunisian shrub desert are reported. The workers search singly for their food (mostly animal carcasses) and are singleprey loaders. The individuals differ to a great extent in their persistence to re-search the place of a find on a previous foraging excursion. The differences range continuously from thoroughly researching a place to just walking by. If, in an experiment, the same reward is offered farther from the nest, each ant persists more in re-searching the place than if food is offered close to the nest. In a further experiment, some individuals persisted less in searching near the former finding site if they had collected a fly than after collecting a piece of cheese. There is, however, evidence that individuals do not differ in their food preference. Persistent individuals, which re-search the place of a former find, are faster than non-persistent ones in retrieving food that is experimentally arranged in an aggregated manner. The experiment failed to demonstrate the (reverse) superiority of non-persistent individuals foraging on homogeneously distributed food. The observations of unmanipulated foraging excursions in the field suggest such an advantage for non-persistent foragers under natural conditions where food in general occurs widely dispersed. The colony as a whole retrieves more food within the same time from an experimental lay-out that is homogeneous than from an aggregated one. The behavioural differences between individuals could be caused by a training bias of the short-lived foragers, leading to a different assessment of the profitability of a searching method which implies returning to a formerly rewarding place. Thus, each worker uses the most promising behaviour according to its individual experience. Alternatively, the individually different searching methods could mainly contribute to the welfare of the colony as a whole rather than leading to a maximal short-term efficiency of each individual. In particular, the colony, disposing of only a few highly persistent foragers, could quickly exploit occasional short-lived, but unpredictible, clumps of food within its foraging range.     

Queen number and the production of sexuals in the fire ant,Solenopsis invicta (Hymenoptera: Formicidae)

Summary To investigate the possibility of queen control over the production of sexuals in polygyne colonies of the fire ant, Solenopsis invicta, large colonies were divided into polygyne (P) and monogyne (M) or queenless (Q-) halves. Sexual larvae were evident in the M and Q- halves 3 to 4 days after colony division, whereas sexual forms failed to develop in all but one of the 32 P halves examined. Both male and female sexuals were produced in abundance in all M (n=25) and Q- (n=7) halves. Evidently, individuals capable of sexualization are present in colonies with many functional queens but are normally prevented from developing. Electrophoretic and morphometric analyses indicated that both haploid and diploid males were produced in the Q- halves, although diploids far outnumbered haploids. It thus appears that queens exert control over all potential and genetically determined sexuals regardless of sex or ploidy. The timing of the appearance of sexual forms following colony division suggests that queen control may be pheromonally mediated and inhibits the growth of sexuals late in larval development. An experiment in which the queens from M and P halves of colonies were exchanged demonstrated the reversible nature of this inhibition within colonies, but also suggested that once individual larvae develop beyond a critical point they are no longer subject to queen control. Despite seasonal variation in the production of sexuals in the field, no substantial differences between colonies collected in the summer and fall were found in their response to colony manipulations. The interaction of colony weight and number of queens present prior to colony division was associated with the number of males produced in the Q- halves, but no factors examined were associated with the number of females produced in these halves, or with the number of males or females produced in the M halves.     

Lack of detectable nepotism in multiple-queen colonies of the fire ant Solenopsis invicta (Hymenoptera: Formicidae)

Multiple-queen (polygyne) colonies of the introduced fire ant Solenopsis invicta present a paradox for kin selection theory. Egg-laying queens within these societies are, on average, unrelated to one another, and the numbers of queens per colony are high, so that workers appear to raise new sexuals that are no more closely related to them than are random individuals in the population. This paradox could be resolved if workers discriminate between related and unrelated nestmate sexuals in important fitness-related contexts. This study examines the possibility of such nepotism using methods that combine the following features: (1) multiple relevant behavioral assays, (2) colonies with an unmanipulated family structure, (3) multiple genetic markers with no known phenotypic effects, and (4) a statistical technique for distinguishing between nepotism and potentially confounding phenomena. We estimated relatedness between interactants in polygyne S. invicta colonies in two situations, workers tending egg-laying queens and workers feeding maturing winged queens. In neither case did we detect a significant positive value of relatedness that would implicate nepotism. We argue that the non-nepotistic strategies displayed by these ants reflect historical selection pressures experienced by native populations, in which nestmate queens are highly related to one another. The markedly different genetic structure in native populations may favor the operation of stronger higher-level selection that effectively opposes weaker individual-level selection for nepotistic interactions within nests. Received: 28 June 1996 / Accepted after revision: 6 October 1996     

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.     

The effect of colony size and starvation on food flow in the fire ant,Solenopsis invicta (Hymenoptera: Formicidae)

Summary Food-sharing experiments were performed with laboratory colonies of Solenopsis invicta containing 1000, 10,000, or 20,000 workers and starved for 0, 3, 7, or 14 days. The effect of these variables was measured on the uptake of radioactive sugar water (1 M) by 1% of the colony's workers and on the trophallactic flow of food from these foragers to the remainder of the colony.Patterns of food distribution in small colonies differed significantly from those in larger nests. In 1000-ant nests, small workers more frequently received food than large workers, but in bigger colonies the opposite occurred.Fire ants were adept at distributing sugar water, with food from a few workers rapidly reaching the majority of the colony as foragers donate their crop contents to groups of recipients and these recipients may themselves act as donors.Foragers respond to colony starvation by individually taking up more food and sharing this fluid with a greater proportion of nestmates. Even foragers from satiated colonies can retrieve at least small amounts of liquid.The forager's state of hunger plays an important role in regulating food distribution. In sugar-satiated nests, previously starved foragers are highly successful at passing on labelled sugar whereas prviously fed foragers are not.