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.     

Social organization in the ant Pheidole dentata

Summary Caste theory states that the proportions of individuals in different demographic classes of an insect society should vary with environmental factors, and are adaptive because they enhance colony-level efficiency. We examined the proportions of workers in different age and size classes (temporal and physical castes) in whole colonies of the ant Pheidole dentata collected in two different habitats. Despite significant ecological differences between the habitats in competition, resource availability and predation, we found no differences in the physical and temporal caste structures of colonies. Also, there was no correlation between physical or temporal caste ratios and the reproductive output of colonies. Because of topography, distance between sites, and apparent low vagility of Pheidole alates, we assume that gene flow between the sites is inadequate to account for the observed similarities. Although age- and size-related patterns of division of labor were observed, similarities in the behavioral profiles (the sum of the relative contributions of each age cohort to the performance of tasks) in colonies having different age caste structures suggests that worker, flexibility may be more important than rigidly programmed age- and size-correlated patterns of task performance.     

Colony genetic diversity affects task performance in the red ant Myrmica rubra

High relatedness and low genetic diversity among individuals in a group is generally considered crucial to the evolution of cooperative behaviour. However, in about a third of social insect species, intracolonial genetic diversity is increased because of derived polyandry (multiple mating by queens) and/or polygyny (multiple reproductive queens). Several studies have shown that increased intracolonial genetic diversity can enhance task performance in honey bees, but evidence of such effect in other social insects is still lacking. Why increased genetic diversity has evolved in some, but not all species, is a fundamental question in sociobiology. In this study, we investigated the effect of intracolonial genetic diversity on the task of nest migration, using the facultatively polyandrous and polygynous red ant Myrmica rubra. Genetic diversity significantly affected migration speed, but its effects were context dependent. Migration speed correlated positively with genetic diversity in one experiment in which migrations were into a known nest site, due to quicker transfer of brood into the new nest once consensus was reached. However, in a another experiment in which migration included scouting for new nest sites, migration speed correlated negatively with genetic diversity, due to slower discovery of new nest sites and slower transfer of brood into the new nest. Our results show for the first time that genetic diversity affects task performance in a social insect other than the honeybee, but that it can produce contrasting effects under different conditions.     

Dual mechanism of queen influence over sex ratio in the ant Pheidole pallidula

Social Hymenoptera are general models for the study of parent-offspring conflict over sex ratio, because queens and workers frequently have different reproductive optima. The ant Pheidole pallidula shows a split distribution of sex ratios with most of the colonies producing reproductives of a single sex. Sex ratio specialization is tightly associated with the breeding system, with single-queen (monogynous) colonies producing male-biased brood and multiple-queen (polygynous) colonies female-biased brood. Here, we show that this sex specialization is primarily determined by the queens influence over colony sex ratio. Queens from monogynous colonies produce a significantly more male-biased primary sex ratio than queens from polygynous colonies. Moreover, queens from monogynous colonies produce a significantly lower proportion of diploid eggs that develop into queens and this is associated with lower rate of juvenile hormone (JH) production compared to queens from polygynous colonies. These results indicate that queens regulate colony sex ratio in two complementary ways: by determining the proportion of female eggs laid and by hormonally biasing the development of female eggs into either a worker or reproductive form. This is the first time that such a dual system of queen influence over colony sex ratio is identified in an ant.     

Pheromone trails in the Brazilian ant Pheidole oxyops: extreme properties and dual recruitment action

Communication of feeding locations is widespread in social animals. Many ants use pheromone trails to guide nestmates to food sources, but trail properties and how they are used vary. The ant Pheidole oxyops retrieves prey cooperatively using multiple workers. The recruited workers are guided to the prey by a pheromone trail laid by the initial discoverer. In comparison to other ants, this trail has extreme properties. Despite being laid by just one ant, freshly laid trails are followed very accurately (84.4?% correct choices at a bifurcation), but decay in only 5–7?min. This extreme accuracy and short duration probably reflect adaptations to underlying differences in feeding ecology. In particular, P. oxyops needs to rapidly recruit nestmates to a precise location in a competitive environment. Rapid decay combined with a natural walking speed of 1.4?m/min should set an upper limit of 4?m (an 8-m round trip) on recruitment range. However, experimentally placed food items up to 8?m from the nest entrance were cooperatively retrieved. This greater range is due to the trail having a dual recruitment role. It not only recruits from the nest but also intercepts ants already outside the nest, causing them to join the trail. Seventy-five per cent of ants joining the trail then followed it towards the food item. Even when direct recruitment from the nest was prevented, this secondary recruitment action resulted in seven times as many ants locating a food source than by chance discovery and in items being moved 46?% sooner.     

The relation between caste ratios and division of labor in the ant genus Pheidole (Hymenoptera: Formicidae)

Summary Ten species of Pheidole, representing as many species groups from various localities in North and South America, Asia, and Africa, were analyzed to probe for possible relationships between caste ratios and division of labor.Minor workers are behaviorally almost uniform among the species, but major workers vary in repertory from 4 to 19 behavioral acts (Table 1, Fig. 2). The major repertory size increases significantly across the species with the percentage of majors in the worker force (Fig. 3). This trend is consistent with the basic prediction of ergonomic optimization models under an assumption of colony-level selection. There is also a trend toward reduction of behavioral repertory with increase of size in the major relative to the minor, a second relation expected from theory, but the data are not sufficient to reach statistical significance.When the minor:major ratio was lowered to below 1:1 (from the usual 3:1 to 20:1, according to species), in three widely different species (guilelmimuelleri, megacephala, pubiventris), the repertory size increased by 1.4–4.5X and the rate of activity by 15–30X (Table 1, Figs. 4–6). The change occurred within 1 h of the ratio change and was reversed in comparably short time when the original ratio was restored.This abrupt and important shift in behavior permitted the major workers to serve as an emergency stand-by caste, available to be summoned to a nearly full repertory when the minor worker caste was depleted. The majors also restored 75% or more of the missing minor workers' activity rate under laboratory conditions. Their transformation allowed continued oviposition by the queen and the rearing of larvae to the adult stage.In line with these findings, a distinction is made between programmed elasticity in the repertory of individual workers and castes and the resiliency of the colony as a whole, which depends upon the pattern of caste-specific elasticity.     

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.     

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.     

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.     

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

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

Age,experience and reproductive performance in a long-lived bird: a hormonal perspective

The ultimate factors influencing age-specific reproductive performance in birds have been widely discussed, and several hypotheses have been suggested to explain why young/inexperienced breeders have lower reproductive success than older individuals. In comparison, proximate factors and, particularly, hormonal mechanisms influencing age-related reproductive performance have received lesser attention. In this paper, we examined how baseline levels of corticosterone and prolactin, two hormones involved in reproduction, changed with age and experience in a long-lived bird, the Black-browed albatross (Thallasarche melanophris) during the brooding stage. Corticosterone levels were not linked to age, whereas prolactin levels increased until individuals reached 15 years of age. First-time breeders had higher corticosterone levels and lower prolactin levels than experienced ones. Corticosterone levels were not correlated with breeding experience among experienced birds, whereas prolactin levels slightly increased with advancing experience. Among experienced breeders, there was no effect of individual quality on corticosterone and prolactin levels. Baseline corticosterone and prolactin levels were respectively, positively and negatively correlated to time spent fasting/brooding on the nest. Moreover, the probability of successfully fledging a chick was negatively related to corticosterone levels, but not to prolactin levels. Elevated corticosterone levels in first time breeders may serve as evidence for depleted body reserves resulting from lower foraging/brooding capabilities and therefore support the constraint hypothesis. Low prolactin levels in young/inexperienced birds may be interpreted either as evidence for their lower breeding capacities (constraint hypothesis) or for their limited breeding investment (restraint hypothesis). Finally, we report, for the first time, the hormonal changes associated with the onset of senescence. The very old and most experienced birds, which had the lowest probability of successfully fledging a young, displayed elevated corticosterone levels and low prolactin levels, possibly indicating a degradation of breeding skills and/or a disruption of the endocrine system in senescent birds.     

The red and the black: habituation and the dear-enemy phenomenon in two desert Pheidole ants

Many species of territorial animals are more aggressive toward strangers than neighbors, a pattern of aggression referred to as the ’dear-enemy phenomenon.’ In many cases, the mechanism by which neighbors are discriminated from strangers and the function of neighbor-stranger discrimination remain controversial. We investigated the spatial patterns of inter-colony aggression within and between two Pheidole species of seed-harvesting ants in the Mojave Desert of California by quantifying aggression between colonies in standardized staged encounters. We also tested whether the level of fighting between workers of two colonies is affected by previous exposure to each other. We show that neighbors (i.e., colonies less that 2.6 m away) of either species are treated less aggressively than more distant colonies and that habituation may be a mechanism by which this discrimination is achieved. The variation in aggression among spatially distant colonies also suggests that additional genetic or environmental factors are involved in recognition. The function of the dear-enemy phenomenon in these ant species may be related to the greater risk to the resources of a colony presented by strange workers than workers from a neighboring colony. Received: 18 November 1999 / Received in revised form: 3 April 2000 / Accepted: 3 May 2000     

Experimental manipulation of colony genetic diversity had no effect on short-term task efficiency in the Argentine ant Linepithema humile

Genetic diversity might increase the performance of social groups by improving task efficiency or disease resistance, but direct experimental tests of these hypotheses are rare. We manipulated the level of genetic diversity in colonies of the Argentine ant Linepithema humile, and then recorded the short-term task efficiency of these experimental colonies. The efficiency of low and high genetic diversity colonies did not differ significantly for any of the following tasks: exploring a new territory, foraging, moving to a new nest site, or removing corpses. The tests were powerful enough to detect large effects, but may have failed to detect small differences. Indeed, observed effect sizes were generally small, except for the time to create a trail during nest emigration. In addition, genetic diversity had no statistically significant impact on the number of workers, males and females produced by the colony, but these tests had low power. Higher genetic diversity also did not result in lower variance in task efficiency and productivity. In contrast to genetic diversity, colony size was positively correlated with the efficiency at performing most tasks and with colony productivity. Altogether, these results suggest that genetic diversity does not strongly improve short-term task efficiency in L. humile, but that worker number is a key factor determining the success of this invasive species.Communicated by L. Sundström     

Division of labour in a crisis: task allocation during colony emigration in the ant Leptothorax unifasciatus (Latr.)

Division of labour during colony emigration is widespread in ants. An important problem is how tasks are allocated during colony movement from one nest site to another. The generally favoured view is that emigrations are organised by a minority group of individuals, which either work unusually hard at tasks (elites) or have the exclusive task of carrying out the emigration (moving specialists). Five consecutive emigrations of a Leptothorax unifasciatus (Latr.) colony showed that the number of transporters, i.e. the individuals that took an active part in the emigration by transporting brood and ants, was smaller than it would have been if allocation of this task was random during each emigration. However, single emigrations of another three colonies, for which the spatial distribution and behaviour of the workers had been observed for a week prior to the emigration, demonstrated that the transporters did not form a homogeneous group. They differed in their spatial positions and tasks before the emigration. There was also no evidence that transporters worked harder or less hard than their nestmates before the emigration. Therefore, the individuals which carry out emigrations in L. unifasciatus colonies appear to be neither moving specialists nor elites. We propose that task allocation during emigrations of L. unifasciatus colonies is based on a feedback mechanism that involves learning.     

Colony-level selection effects on individual and colony foraging task performance in honeybees, Apis mellifera L.

In honeybees, as in other highly eusocial species, tasks are performed by individual workers, but selection for worker task phenotypes occurs at the colony level. We investigated the effect of colony-level selection for pollen storage levels on the foraging behavior of individual honeybee foragers to determine (1) the relationship between genotype and phenotypic expression of foraging traits at the individual level and (2) how genetically based variation in worker task phenotype is integrated into colony task organization. We placed workers from lines selected at the colony level for high or low pollen stores together with hybrid workers into a common hive environment with controlled access to resources. Workers from the selected lines showed reciprocal variation in pollen and nectar collection. High-pollen-line foragers collected pollen preferentially, and low- pollen-line workers collected nectar, indicating that the two tasks covary genetically. Hybrid workers were not intermediate in phenotype, but instead showed directional dominance for nectar collection. We monitored the responses of workers from the selected strains to changes in internal (colony) and external (resource) stimulus levels for pollen foraging to measure the interaction between genotypic variation in foraging behavior and stimulus environment. Under low-stimulus conditions, the foraging group was over-represented by high-pollen-line workers. However, the evenness in distribution of the focal genetic groups increased as foraging stimuli increased. These data are consistent with a model where task choice is a consequence of genetically based response thresholds, and where genotypic diversity allows colony flexibility by providing a range of stimulus thresholds. Received: 3 May 1999 / Received in revised form: 22 December 1999 / Accepted: 23 January 2000     

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.     

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.