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     

Division of labor in honeybees: form, function, and proximate mechanisms

Honeybees exhibit two patterns of organization of work. In the spring and summer, division of labor is used to maximize growth rate and resource accumulation, while during the winter, worker survivorship through the poor season is paramount, and bees become generalists. This work proposes new organismal and proximate level conceptual models for these phenomena. The first half of the paper presents a push–pull model for temporal polyethism. Members of the nursing caste are proposed to be pushed from their caste by the development of workers behind them in the temporal caste sequence, while middle-aged bees are pulled from their caste via interactions with the caste ahead of them. The model is, hence, an amalgamation of previous models, in particular, the social inhibition and foraging for work models. The second half of the paper presents a model for the proximate basis of temporal polyethism. Temporal castes exhibit specialized physiology and switch caste when it is adaptive at the colony level. The model proposes that caste-specific physiology is dependent on mutually reinforcing positive feedback mechanisms that lock a bee into a particular behavioral phase. Releasing mechanisms that relate colony level information are then hypothesized to disrupt particular components of the priming mechanisms to trigger endocrinological cascades that lead to the next temporal caste. Priming and releasing mechanisms for the nursing caste are mapped out that are consistent with current experimental results. Less information-rich, but plausible, mechanisms for the middle-aged and foraging castes are also presented.     

Brood temperature, task division and colony survival in honeybees: A model

One of the mechanisms by which honeybees regulate division of labour among their colony members is age polyethism. Here the younger bees perform in-hive tasks such as heating and the older ones carry out tasks outside the hive such as foraging. Recently it has been shown that the higher developmental temperatures of the brood, which occur in the centre of the brood nest, reduce the age at which individuals start to forage once they are adult. It is unknown whether this effect has an impact on the survival of the colony. The aim of this paper is to study the consequences of the temperature gradient on the colony survival in a model on the basis of empirical data.We created a deterministic simulation of a honeybee colony (Apis mellifera) which we tuned to our empirical data. In the model in-hive bees regulate the temperature of the brood nest by their heating activities. These temperatures determine the age of first foraging in the newly emerging bees and thus the number of in-hive bees present in the colony. The results of the model show that variation in the onset of foraging due to the different developmental temperatures has little impact on the population dynamics and on the absolute number of bees heating the nest unless we increase this effect by several times to unrealistic values, where individuals start foraging up to 10 days earlier or later. Rather than on variation in the onset of foraging due to the temperature gradient it appears that the survival of the colony depends on a minimal number of bees available for heating at the beginning of the simulation.     

Evolution of self-organized division of labor in a response threshold model

Division of labor in social insects is determinant to their ecological success. Recent models emphasize that division of labor is an emergent property of the interactions among nestmates obeying to simple behavioral rules. However, the role of evolution in shaping these rules has been largely neglected. Here, we investigate a model that integrates the perspectives of self-organization and evolution. Our point of departure is the response threshold model, where we allow thresholds to evolve. We ask whether the thresholds will evolve to a state where division of labor emerges in a form that fits the needs of the colony. We find that division of labor can indeed evolve through the evolutionary branching of thresholds, leading to workers that differ in their tendency to take on a given task. However, the conditions under which division of labor evolves depend on the strength of selection on the two fitness components considered: amount of work performed and on worker distribution over tasks. When selection is strongest on the amount of work performed, division of labor evolves if switching tasks is costly. When selection is strongest on worker distribution, division of labor is less likely to evolve. Furthermore, we show that a biased distribution (like 3:1) of workers over tasks is not easily achievable by a threshold mechanism, even under strong selection. Contrary to expectation, multiple matings of colony foundresses impede the evolution of specialization. Overall, our model sheds light on the importance of considering the interaction between specific mechanisms and ecological requirements to better understand the evolutionary scenarios that lead to division of labor in complex systems. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1007/s00265-012-1343-2) contains supplementary material, which is available to authorized users.     

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     

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.     

Reward rate and forager activation in honeybees: recruiting mechanisms and temporal distribution of arrivals

We analyzed the foraging and recruitment activity of single foragers ( Apis mellifera), exploiting low reward rates of sucrose solution. Single employed foragers (test bees) were allowed to collect 2.0 m sucrose solution delivered by a rate-feeder located at 160 m from the hive for 2 h. Flow rates varied between 1.4 and 5.5 µl/min. The individual behavior of the test bees was registered both at the hive and the food source, and the social output was calculated as the number of incoming bees arriving at the feeder per hour (henceforth: arrival rate). Incoming bees were captured once they landed at the feeder and assigned to one of three categories according to their foraging experience and hive interactions with the test bee: inspector, reactivated, or inexperienced bees. Both the waggle-runs performed per hour of foraging by test bees and the social output attained, increased with the reward rate. Also the number of hive-stays and the trophallactic-offering contacts performed by test bees were positively correlated with the arrival rate. For the highest reward rates, the duration of Nasonov-gland exposure at the feeding place was higher, and the arrival of most of the incoming bees occurred shortly after the test bee landed at the feeding platform. Thus, in addition to hive-interactions, landing of incoming bees at the food source is promoted by olfactory and/or visual information provided by the test bees. The proportions of inspector, reactivated, and inexperienced bees changed depending on the reward rate offered. Therefore, not only the occurrence and intensity of the recruitment-related behaviors performed by the test bees, but also the stimulation required by each category of incoming bees, determined the social output observed.     

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.     

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).     

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.     

Division of labor in a dynamic environment: response by honeybees (Apis mellifera) to graded changes in colony pollen stores

 A fundamental requirement of task regulation in social groups is that it must allow colony flexibility. We tested assumptions of three task regulation models for how honeybee colonies respond to graded changes in need for a specific task, pollen foraging. We gradually changed colony pollen stores and measured behavioral and genotypic changes in the foraging population. Colonies did not respond in a graded manner, but in six of seven cases showed a stepwise change in foraging activity as pollen storage levels moved beyond a set point. Changes in colony performance resulted from changes in recruitment of new foragers to pollen collection, rather than from changes in individual foraging effort. Where we were able to track genotypic variation, increases in pollen foraging were accompanied by a corresponding increase in the genotypic diversity of pollen foragers. Our data support previous findings that genotypic variation plays an important role in task regulation. However, the stepwise change in colony behavior suggests that colony foraging flexibility is best explained by an integrated model incorporating genotypic variation in task choice, but in which colony response is amplified by social interactions. Received: 17 October 1998 / Received in revised form: 11 March 1999 / Accepted: 12 March 1999     

Habitat structure helps guide the emergence of colony-level personality in social spiders

Studying the environmental factors that guide the emergence of collective behaviors is instrumental to understanding the ecology and evolution of animal societies. Although recent work has provided insights into the demographic factors that influence inter-colony variation in collective behavior (i.e., colony-level personality or collective personality), relatively few studies have investigated how the physical environment (e.g., habitat structure) affects colony-level personality. Here, we study the emergence of collective personality in prey capture behavior in the social spider, Stegodyphus dumicola. We measured collective prey capture behavior four times over 36 days in a classic repeated measures design. We used four different artificial habitat (web support) structures in three different treatments: habitat structure was either (1) fixed and undisturbed, (2) disturbed with a complete removal of webbing between each measurement, or (3) disturbed with changes of habitat structure between each measurement. Our results revealed that repeatability in colony-level personality was retained as long as habitat structure was not altered. However, the repeatability of colony-level personality declined precipitously when groups were forced to build their webs on novel habitat structures. Furthermore, habitat structure affected collective capture behavior, that is, latency to attack and the number of attackers differed among colonies on different habitat structures. Collectively, our data demonstrate that habitat structure is instrumental in shaping both the mean and repeatability of the collective behavior of colonies and may influence overall foraging success.     

Division of labor between scouts and recruits: genetic influence and mechanisms

Every recruitment system in social insects requires some individuals that serve as scouts, foragers that search independently for food sources. It is not well understood which factors influence whether an individual becomes a scout or a recruit, nor how the division of labor between the two forager groups is regulated. It is shown here for honeybees (Apis mellifera), using two different molecular techniques, that there is a genetically based difference in the probability that individuals will scout independently for food. In contrast to earlier suggestions, experimental tests showed that the age of a bee does not seem to influence its probability of becoming a scout or a recruit. Furthermore, scout bees do not search opportunistically for either pollen or nectar but, rather, individuals have preferences that are genetically based. These findings are discussed in the framework of foraging regulation by specialization in honeybees and the adaptive significance of polyandry. Received: 23 October 1997 / Accepted after revision: 10 April 1998     

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.     

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.