Emergence of increased division of labor as a function of group size

Empirical evidence suggests that division of labor in insect societies is positively related to group size both within and across taxa. Response threshold models (RTM) have been commonly used to analyze patterns of division of labor. However, these models have been explored empirically and theoretically for only a limited number of tasks, and few studies have examined predictions of the model as colony size and work availability change. We theoretically examine how group size influences division of labor using a fixed response-threshold model. We simultaneously explore how expected by-products of increased colony size, including demand (total work need relative to total work force available) and task number, affect this relationship. Our results indicate that both low demand and high task number positively influence division of labor. We suggest that these changes parallel what is observed within social groups as their size increases, and that, in part, the commonly observed increased division of labor with increasing group size is emergent.     

Optimal biomass allocation in heterogeneous environments in a clonal plant—Spatial division of labor

When interconnected ramets of clonal plants are growing in heterogeneous environments, ramets may specialize to uptake locally abundant resources rather than scarce resources. This biomass allocation pattern may result in more efficient sharing of resources through physiological integration and an overall benefit to the plants (spatial division of labor; DoL).     

Response thresholds to sucrose predict foraging division of labor in honeybees

Division of labor, where thousands of individuals perform specific behavioral acts repeatedly and non-randomly, is the hallmark of insect societies. Virtually nothing is known about the underlying neurophysiological processes that direct individuals into specific behavioral roles. We demonstrate that sensory-physiological variation in the perception of sucrose in honeybees measured when they are 1 week old correlates with their foraging behavior 2–3 weeks later. Workers with the lowest response thresholds became water foragers, followed with increasing response thresholds by pollen foragers, nectar foragers, bees collecting both pollen and nectar, and finally those returning to the colony empty (water<pollen<nectar<both<empty). Sucrose concentrations of nectar loads were positively correlated with response thresholds measured on 1-week-old bees. These results demonstrated how the variable response thresholds of a sensory-physiological process, the perception of sucrose, is causally linked to the division of labor of foraging. Received. 28 June 1999 / Received in revised form: 2 November 1999 / Accepted: 20 November 1999     

Regulation of honey bee division of labor by colony age demography

The age at which worker honey bees begin foraging varies under different colony conditions. Previous studies have shown that juvenile hormone (JH) mediates this behavioral plasticity, and that worker-worker interactions influence both JH titers and age at first foraging. These results also indicated that the age at first foraging is delayed in the presence of foragers, suggesting that colony age demography directly influences temporal division of labor. We tested this hypothesis by determining whether behavioral or physiological development can be accelerated, delayed, or reversed by altering colony age structure. In three out of three trials, earlier onset of foraging was induced in colonies depleted of foragers compared to colonies depleted of an equal number of bees across all age classes. In two out of three trials, delayed onset of foraging was induced in colonies in which foragers were confined compared to colonies with free-flying foragers. Finally, in three out of three trials, both endocrine and exocrine changes associated with reversion from foraging to brood care were induced in colonies composed of all old bees and devoid of brood; JH titers decreased and hypopharyngeal glands regenerated. These results demonstrate that plasticity in age-related division of labor in honey bee colonies is at least partially controlled by social factors. The implications of these results are discussed for the recently developed ‘‘activator-inhibitor” model for honey bee behavioral development. Received: 8 November 1995/Accepted after revision: 10 May 1996     

Individual-level patterns of division of labor in honeybees highlight flexibility in colony-level developmental mechanisms

Honeybee division of labor (DOL) has become a model system for exploring the genetic basis of complex traits and phenotypic plasticity. Although many highly informative behavioral studies have been conducted on this topic (both at the cohort and individual levels), most studies have focused on a few behavioral acts, such as the age of first foraging. Few studies have recorded large numbers of relatively complete individual-level patterns of DOL. Such fine-scale patterns would lay the foundation for rigorous molecular analyses of this phenomenon and allow us to differentiate between competing mechanistic models of DOL. Here, we record over 100 individual-level DOL patterns of bees living under natural conditions. We found that the transitions between castes (polyphenism states) are often gradual, with bees being in multiple castes at once. This is contrary to the traditional view that changes are abrupt. We also found that bees often skip castes, a key prediction of a recent model of DOL. We further confirm variation in the rate at which bees pass through castes and the age of first foraging. Taken together, these results greatly improve our understanding of this model system and allow for a strong revision of current models of honeybee DOL.     

Obligate parthenogenesis and reproductive division of labor in the Japanese queenless ant Pristomyrmex pungens

Summary Two types of workers were recognized in colonies of Pristomyrmex pungens: extranidal workers (which characteristically walk outside the nest) and intranidal workers (which characteristically stay inside the nest). The ovaries of extranidal workers showed little activity, whereas those of intranidal workers showed high activity and often contained mature oocytes. I therefore conclude that only the intranidal workers reproduce. A behavioral repertoire of 103 individuals was obtained and used to infer group subdivision using cluster analysis; in addition, principal component analysis was performed on the intranidal workers in this set. These data enabled objective separation of extranidal and intranidal workers. Intranidal workers were larger in size on average than extranidal workers; however, the distributions overlapped. Three tests for further subdivision within the group of intranidal workers indicated that such subdivision is weak, and it is also likely that all intranidal workers lay eggs. There was no significant correlation between body size and reproductive status. The number of mature oocytes per ant fitted a Poisson distribution, and the first two principal component factors scores of behavior showed significant correlation with head width. All extranidal workers had resorbed ovaries and also had yellow bodies (which indicated a history of oviposition). When and how the differentiation between the reproductive intranidal workers and the non-reproductive extranidal workers occurred is discussed. The best-supported hypothesis is that extranidal workers are old intranidal ones. Neither males nor inseminated workers were found in any smaples collected in the field or studied in the laboratory, which greatly strengthens earlier suggestions that Pristomyrmex pungens is the first-known ant to be obligately thelytokous. These findings indicate that Pristomyrmex pungens is no longer eusocial, although it has the highest form of social behavior of any thelytokous species; they also raise the question of whether or not there are factors promoting the loss of eusociality and sexuality in this species. Ecological factors are tentatively indicated, namely, the need to maintain large colonies in the face of a nomadic lifestyle involving frequent colony fragmentation.     

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.     

Timekeeping in the honey bee colony: integration of circadian rhythms and division of labor

The daily patterns of task performance in honey bee colonies during behavioral development were studied to determine the role of circadian rhythmicity in age-related division of labor. Although it is well known that foragers exhibit robust circadian patterns of activity in both field and laboratory settings, we report that many in-hive tasks are not allocated according to a daily rhythm but rather are performed 24 h per day. Around-the-clock activity at the colony level is accomplished through the performance of some tasks by individual workers randomly with respect to time of day. Bees are initially arrhythmic with respect to task performance but develop diel rhythmicity, by increasing the occurrence of inactivity at night, prior to becoming foragers. There are genotypic differences for age at onset of rhythmicity and our results suggest that these differences are correlated with genotypic variation in rate of behavioral development: genotypes of bees that progressed through the age polyethism schedule faster also acquired behavioral rhythmicity at an earlier age. The ontogeny of circadian rhythmicity in honey bee workers ensures that essential in-hive behaviors are performed around the clock but also allows the circadian clock to be engaged before the onset of foraging. Received: 6 October 1997 / Accepted after revision: 28 March 1998     

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.     

Effects of intracolony variability in behavioral development on plasticity of division of labor in honey bee colonies

There is a genetic component to plasticity in age polyethism in honey bee colonies, such that workers of some genotypes become precocious foragers more readily than do workers of other genotypes, in colonies lacking older bees. Using colonies composed of workers from two identifiable genotype groups, we determined that intracolony differences in the likelihood of becoming a precocious forager are a consequence of differences in rates of behavioral development that are also evident under conditions leading to normal development. An alternative hypothesis, that differences in the likelihood of becoming a precocious forager are due to differences in general sensitivity to altered colony conditions, was not supported. In three out of three trials, workers from the genotype group that was more likely to exhibit precocious foraging in single cohort colonies also foraged at relatively younger ages in colonies in which workers exhibited normal behavioral development. In contrast, in three out of three trials, workers from the genotype group that was more likely to exhibit precocious foraging in single-cohort colonies did not show disproportionately more overaged nursing in colonies in which workers exhibited delayed development. These results indicate that genotypic differences in plasticity in age-related division of labor are based on genotypic differences in rates of behavioral development.     

Behavioral and life-history components of division of labor in honey bees (Apis mellifera L.)

Variability exists among worker honey bees for components of division of labor. These components are of two types, those that affect foraging behavior and those that affect life-history characteristics of workers. Variable foraging behavior components are: the probability that foraging workers collect (1) pollen only; (2) nectar only; and (3) pollen and nectar on the same trip. Life history components are: (1) the age the workers initiate foraging behavior; (2) the length of the foraging life of a worker; and (3) worker length of life. We show how these components may interact to change the social organization of honey bee colonies and the lifetime foraging productivity of individual workers. Selection acting on foraging behavior components may result in changes in the proportion of workers collecting pollen and nectar. Selection acting on life-history components may affect the size of the foraging population and the distribution of workers between within nest and foraging activities. We suggest that these components define possible sociogenic pathways through which colony-level natural selection can change social organization. These pathways may be analogous to developmental pathways in the morphogenesis of individual organisms because small changes in behavioral or life history components of individual workers may lead to major changes in the organizational structure of colonies. Correspondence to: R.E. Page, Jr.     

The territoriality threshold: a model for mutual avoidance in dragonfly mating systems

Summary In anisopteran dragonflies a variety of mating systems occurs. Male strategies range from patrolling without site attachment to territorial behaviour with pronounced residentiality. Conceiving site attachment as a strategy of mutual avoidance that reduces the energy spent in intermale fights, we develop a model for the cost and benefit of territoriality. This model suggests that high male density, high inter-male aggressiveness, and short duration of female visits at the mating place will strongly favour localization of males at the mating place and may thus trigger the evolution of territoriality. The predictions of our model are supported by field observations of several dragonfly species.died July 27, 1986     

Competition and cooperation: bumblebee spatial organization and division of labor may affect worker reproduction late in life

Within-group conflict may influence the degree to which individuals within a group cooperate. For example, the most dominant individuals within a group often gain access to the best resources and may be less inclined to perform risky tasks. We monitored space use and division of labor among all workers in three colonies of bumblebees, Bombus impatiens, during the ergonomic and queenless phases of their colony cycle. We then measured the two largest oocytes in each worker to estimate each individual's reproductive potential at the end of the colony cycle. We show that workers that remained farther from the queen while inside the nest and avoided risky or more energy-expensive tasks during the ergonomic phase developed larger oocytes by the end of the colony cycle. These individuals also tended to be the largest, oldest workers. After the queen died, these workers were more likely than their nestmates to increase brood incubation. Our results suggest that inactive bumblebees may be storing fat reserves to later develop reproductive organs and that the spatial organization of workers inside the nest, particularly the distance workers maintain from the queen, may predict which individuals will later have the greatest reproductive potential in the colony.     

Characterization of bedload intermittency near the threshold of motion using a Lagrangian sediment transport model

At the smallest scales of sediment transport in rivers, the coherent structures of the turbulent boundary layer constitute the fundamental mechanisms of bedload transport, locally increasing the instantaneous hydrodynamic forces acting on sediment particles, and mobilizing them downstream. Near the critical threshold for initiating sediment motion, the interactions of the particles with these unsteady coherent structures and with other sediment grains, produce localized transport events with brief episodes of collective motion occurring due to the near-bed velocity fluctuations. Simulations of these flows pose a significant challenge for numerical models aimed at capturing the physical processes and complex non-linear interactions that generate highly intermittent and self-similar bedload transport fluxes. In this investigation we carry out direct numerical simulations of the flow in a rectangular flat-bed channel, at a Reynolds number equal to Re = 3632, coupled with the discrete element method to simulate the dynamics of spherical particles near the bed. We perform two-way coupled Lagrangian simulations of 48,510 sediment particles, with 4851 fixed particles to account for bed roughness. Our simulations consider a total of eight different values of the non-dimensional Shields parameter to study the evolution of transport statistics. From the trajectory and velocity of each sediment particle, we compute the changes in the probability distribution functions of velocities, bed activity, and jump lengths as the Shields number increases. For the lower shear stresses, the intermittency of the global bedload transport flux is described by computing the singularity or multifr actal spectrum of transport, which also characterizes the widespread range of transport event magnitudes. These findings can help to identify the mechanisms of sediment transport at the particle scale. The statistical analysis can also be used as an ingredient to develop larger, upscaled models for predicting mean transport rates, considering the variability of entrainment and deposition that characterizes the transport near the threshold of motion.     

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.     

Changes in diatom patch-size distribution and degradation in a spatially self-organized intertidal mudflat ecosystem

Self-organized spatial patterns have been proposed as possible indicators for regime shifts in ecosystems. Until now, this hypothesis has only been tested in drylands. Here, we focus on intertidal mudflats where regular spatial patterns develop in early spring from the interaction between diatom growth and sedimentation but disappear when benthic herbivore abundance increases in early summer, accompanied by a dramatic shift to a bare mudflat. We followed the patch-size distributions of diatom biofilms during this degradation process. As time progressed, we found a temporal change in the spatial configuration occurring simultaneously with the loss of the diatom-sediment feedback. This indicates a gradual failure in time of the self-organization process that underlies regular patterning in this ecosystem. The path to degradation co-occurred with the loss of the larger patches in the ecosystem, which resulted in a decrease of the truncation in the patch-size distribution. Hence, our study in mudflat ecosystems confirms the general hypothesis that spatial patterns can provide important clues about the level of degradation. Nevertheless, our study highlights the need for thorough study about the type of spatial patterns and the nature of the underlying feedbacks before a reliable assessment of ecosystem status can be made, as changes in patch-size distribution differed markedly with those observed in other ecosystems.     

Evolution of the fast start response in the cavefish Astyanax mexicanus

The extreme sensory environment of subterranean caves presents an adaptive challenge for troglobitic organisms. Although caves provide distinct selective pressures (e.g., darkness, food scarcity), advantages often come with living in isolated places. The cave-adapted (hypogean) form of the teleost Astyanax mexicanus lacks predators in its natural environment, unlike its ancestral surface (epigean) form that inhabits the nearby rivers. This species provides a unique opportunity for comparative studies because A. mexicanus has invaded the cave environment multiple times, providing us with independent comparative adaptive experiments. Here, we examine kinematic parameters that characterize the escape responses of various forms of A. mexicanus. We demonstrate that populations differ in details of fast start performance, but that surface fish do not perform better than cavefish in escape responses. Our results are more consistent with genetic drift or divergent selection among caves than with relaxation of selection in determining the evolution of escape behavior in this system.     

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.