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).     

Evidence for division of labor in the social caterpillar Eucheira socialis (Lepidoptera: Pieridae)

The caterpillars of Eucheira socialis westwoodi cooperatively spin and maintain a hollow silken nest and an elaborate network of silken foraging trails on their host plant, madrone (Arbutus spp.: Ericaceae). Nests typically contain several hundred larvae. Two populations are known to harbor a sex ratio distorter. The primary sex ratio in these two populations for four generations has been exceedingly male biased (64–79% male). Lepidoptera larvae are easily sexed using external morphology, allowing us to uniquely mark male and female larvae and to assemble larval groups of particular sex ratios. We report here the results of experiments on sex-specific larval behavior and physiology and the effect of colony sex ratio on individual behavior. We found that male larvae spent more time spinning silk on the nest and less time feeding than female larvae. Males were the first to emerge from the nest and the first to venture out along trails to feed. Male-biased nests had a significantly greater amount of silk deposited on their surfaces than female-biased nests. In the field, male-biased nests produced heavier male and female pupae than female-biased nests. Male and female larvae in 75% male nests became active earlier than males and females in other sex ratio treatments. Received: 11 September 1998 / Received in revised form: 24 February 1999 / Accepted: 27 March 1999     

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     

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.     

Why do not all workers work? Colony size and workload during emigrations in the ant Temnothorax albipennis

Here, we study distribution of workload and its relationship to colony size among worker ants of Temnothorax albipennis, in the context of colony emigrations. We find that one major aspect of workload, number of items transported by each worker, was more evenly distributed in larger colonies. By contrast, in small colonies, a small number of individuals perform most of the work in this task (in one colony, a single ant transported 57% of all items moved in the emigration). Transporters in small colonies carried more items to the new nest per individual and achieved a higher overall efficiency in transport (more items moved per transporter and unit time). Our results suggest that small colonies may be extremely dependent on a few key individuals. In studying colony organisation and division of labour, the amount of work performed by each individual, not just task repertoire (which tasks are performed at all), should be taken into account.     

Structure and resilience of the social network in an insect colony as a function of colony size

Social interactions are critical to the organization of worker activities in insect colonies and their consequent ecological success. The structure of this interaction network is therefore crucial to our understanding of colony organization and functioning. In this paper, I study the properties of the interaction network in the colonies of the social wasp Ropalidia marginata. I find that the network is characterized by a uniform connectivity among individuals with increasing heterogeneity as colonies become larger. Important network parameters are found to be correlated with colony size and I investigate how this is reflected in the organization of work in colonies of different sizes. Finally, I test the resilience of these interaction networks by experimental removal of individuals from the colony and discuss the structural properties of the network that are related to resilience in a social network. This contribution is part of the special issue “Social Networks: new perspectives” (Guest Editors: J. Krause, D. Lusseau, and R. James).     

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     

Division of foraging labor in ants can mediate demands for food and safety

Solitary foragers can balance demands for food and safety by varying their relative use of foraging patches and their level of vigilance. Here, we investigate whether colonies of the ant, Formica perpilosa, can balance these demands by dividing labor among workers. We show that foragers collecting nectar in vegetation near their nest are smaller than are those collecting nectar at sites away from the nest. We then use performance tests to show that smaller workers are more likely to succumb to attack from conspecifics but feed on nectar more efficiently than larger workers, suggesting a size-related trade-off between risk susceptibility and harvesting ability. Because foragers that travel away from the nest are probably more likely to encounter ants from neighboring colonies, this trade-off could explain the benefits of dividing foraging labor among workers. In a laboratory experiment, we show that contact with aggressive workers results in an increase in the mean size of recruits to a foraging site: this increase was not the result of more large recruits, but rather because fewer smaller ants traveled to the site. These results suggest that workers particularly susceptible to risk avoid dangerous sites, and suggest that variation in worker size can allow colonies to exploit profitably both hazardous and resource-poor patches.Communicated by L. Sundström     

The control of water collection in honey bee colonies

A honey bee (Apis mellifera) colony adaptively controls the collection of water by its foragers, increasing it when high temperatures necesssitate evaporative cooling inside the hive and decreasing it when the danger of overheating passes. This study analyzes the mechanisms controlling water collection once it has begun, that is, how a colony's water collectors know whether to continue or stop their activity. M. Lindauer suggested that water collectors acquire information about their colony's need for more water by noting how easily they can unload their water to bees inside the hive. In support of this hypothesis, we found that a water collector's ease of unloading does indeed change when her colony's need for water changes. How does a water collector sense the ease of unloading? Multiple variables of the unloading experience change in relation to a colony's water need. Three time-based variables – initial search time, total search time, and delivery time – all change quite strongly. But what changes most strongly is the number of unloading rejections (refusals by receiver bees to take the water), suggesting that this is the primary index of ease of unloading. Why does a water collector's ease of unloading change when her colony's need for water changes? Evidently, what links these two variables is change in the number of water receivers. These are middle-aged bees that receive water just inside the hive entrance, then transport it deeper inside the hive, and finally smear it on the walls of cells or give it to other bees, or both. A colony increases the number of water receivers when its water need increases by having bees engaged in nectar reception and other tasks (and possibly also bees that are not working) switch to the task of water reception. Evidently the activation of additional water receivers does not strongly reduce the number of nectar receivers in a colony, since a colony can increase greatly its water collection without simultaneously decreasing its collection of rich nectar. This study provides a clear example of the way that the members of a social insect colony can use indirect indicators of their colony's labor needs to adaptively control the work that they perform.     

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     

The honey bee’s tremble dance stimulates additional bees to function as nectar receivers

If a forager bee returns to her hive laden with high-quality nectar but then experiences difficulty finding a receiver bee to unload her, she will begin to produce a conspicuous communication signal called the tremble dance. The context in which this signal is produced suggests that it serves to stimulate more bees to function as nectar receivers, but so far there is no direct evidence of this effect. We now report an experiment which shows that more bees do begin to function as nectar receivers when foragers produce tremble dances. When we stimulated the production of tremble dances in a colony and counted the number of bees engaged in nectar reception before and after the period of intense tremble dancing, we found a dramatic increase. In two trials, the number of nectar receivers rose from 17% of the colony’s population before tremble dancing to 30–50% of the population after the dancing. We also investigated which bees become the additional nectar receivers, by looking at the age composition of the receiver bees before and after the period of intense tremble dancing. We found that none of the bees recruited to the task of nectar reception were old bees, most were middle-aged bees, and some were even young bees. It remains unclear whether these auxiliary nectar receivers were previously inactive (as a reserve supply of labor) or were previously active on other tasks. Overall, this study demonstrates that a honey bee colony is able to rapidly and strongly alter its allocation of labor to adapt to environmental changes, and it further documents one of the communication mechanisms underlying this ability. Received: 31 May 1996/Accepted after revision: 9 August 1996     

Time as a constraint on group size in spider monkeys

An animal can only survive in a given habitat if it has enough time to find, process and digest food whilst avoiding predation. The time it has for food acquisition is affected by the vegetation and competition with conspecifics, which depends on aggregation tendencies. We used the relationships between time allocations, on the one hand, and climatic variables (as a proxy for habitat quality) and group size, on the other, to develop a model that predicts maximum ecologically tolerable group size at different locations for spider monkeys. Spider monkeys are particularly interesting because the social communities often split up into small units. Temperature variation and rainfall variation were the main determinants of time budgets. Community size and average annual rainfall determined party size. The model correctly predicted presence or absence of spider monkeys at 78–83% of 217 New World forest sites. Within the geographical range of the species, this time budget model predicted the presence of spider monkeys better than a model based directly on climate variables. Predicted community and party sizes were significantly larger at sites where spider monkeys are present than at sites where they are absent. As required by the model, predicted maximum community sizes were significantly larger than observed community sizes. Moving time showed a U-shaped relationship with party size, which suggests that moving time is the factor that keeps spider monkey communities from travelling together in a tight group.     

Division of labor between undertaker specialists and other middle-aged workers in honey bee colonies

A primary determinant of colony organization in temporally polyethic insect societies is inter-individual variation in behavior that is independent of worker age. We examined behavioral repertoires, behavioral correlates of adult development, and spatial distributions within the hive to explore the mechanisms that produce behavioral variation among middle-age honey bees (Apis mellifera). Individually labeled undertakers, guards, food storers, and wax workers exhibited a broad range of task-related behavior, but bees tagged as undertakers were more likely to subsequently remove a corpse from the hive and handle a corpse compared to other middle-aged bees. The activity level of undertakers was similar to other task groups, suggesting that undertaking specialists were neither hyper-active “elites” nor quiescent “reserves” that become active only when a dead bee stimulus is present. Undertakers also were more likely to remove debris and to remain in the lower region of the hive or near the entrance, even when not engaged in corpse removal; both preferences may promote colony efficiency by reducing inter-task travel times. Guards and undertakers were less likely to perform behavior normally associated with young bees compared to food storers and wax workers. Undertakers and guards also initiated foraging at earlier ages than the other task groups. These results suggest that undertakers and guards may be slightly developmentally advanced compared to food storers and wax workers. There also was evidence for lifetime differences in behavioral preferences which could not be explained by differences in adult development. Bees tagged as undertakers were more likely to subsequently remove a dead bee during their entire pre-foraging career compared to other task groups or members of their general age cohort. Differences in both the rate of adult development and individual behavioral preferences, both of which may be subject to genetic and environmental influences, are important determinants of inter-individual variation among honey bees of middle age. Received: 5 February 1997 / Accepted after revision: 27 May 1997     

The role of age in temporal polyethism in a primitively eusocial wasp

The relation of age to division of labor was assessed in a primitively eusocial wasp, Ropalidia marginata. The performance of four functionally significant tasks was analyzed. It was found that age has a definite correlation with division of labor, since wasps performed tasks in a distinct sequence in their life with successive tasks being initiated at significantly older ages. Age of a wasp was measured in absolute terms and also relative to other individuals in the colony. Probability of performance of a given task relative to other tasks (PTP) and absolute rates at which tasks were performed per unit time (FTP) both showed clear age-dependent patterns, confirming the association of age with division of labor. The proportion of variance explained for both PTP and FTP was significantly higher with relative age than with absolute age. Interindividual interactions were found to be a potential mechanism through which wasps can determine their relative age. The advantages of work organization depending on relative age and the constraints imposed by absolute age are discussed. Received: 2 April 1997 / Accepted after revision: 20 July 1997     

Transmission of a pathogen in Bombus terrestris,with a note on division of labour in social insects

Summary Parasites of social insect workers can be transmitted within the colony to other, related host individuals or, alternatively, to unrelated workers of other colonies. Division of labour affects the probability of transmission, as young individuals often work inside the nest whereas older ones often leave the nest to forage. Therefore, the relative probabilities of transmission within-vs. between-nests is also affected by the delay between host infection and the shedding of propagules, i.e. the latent period of the parasite strain. We therefore hypothesized that strains of the flagellate parasite Crithidia bombi (Trypanosomatidae, Zoomastigophorea) infecting workers of the bumble bee Bombus terrestris (Hymenoptera, Apidae) could differ in their delays and coexist in a population. This would be the case if strains that are shed after a short time delay were more efficiently transmitted to other colony members, whereas strains with long delays were more efficiently transmitted to non-related workers in the population. We tested this hypothesis by experimentally varying time delay and by allowing transmission to either sister workers from the same nest or unrelated workers from other nests. Transmission of C. bombi was measured as the number of parasitic cells shed by the exposed workers after a standard period. The results showed that relatedness as such had no effect, but that delay and nest identity were highly significant effects to explain variation in transmission success. There was a significant interaction between nest identity and delay, such that bees of some colonies acted as efficient transmitters for C. bombi under short delays and vice versa. We discuss how division of labour may affect parasitism in social insects and, vice versa, how division of labour may be under selection from the effects of parasitism, using available evidence from the literature. Correspondence to: P. Schmid-Hempel     

Division of labor and the evolution of task sharing in queen associations of the harvester ant<Emphasis Type="Italic"> Pogonomyrmex californicus</Emphasis>

Division of labor is a key factor in the ecological success of social groups. Recent work suggests that division of labor can emerge even without specific adaptations for task specialization and that it can appear in incipient social groups as a self-organizational property. We investigated experimentally how selection and self-organization may interact during the evolution of division of labor by examining task performance in groups of normally solitary versus normally social ant queens. We created social pairs of colony-founding queens from two populations of the ant Pogonomyrmex californicus, one in which queens are normally solitary and one in which queens form foundress groups, and observed their behavior during nest excavation. In both populations, one of the two queens usually performed most of the excavation, becoming the excavation specialist. We could predict which queen would become the specialist based on their relative propensities to perform the task in other contexts, consistent with a variance-based model of task specialization. The occurrence of specialization even when group members were not adapted to social life suggests that division of labor may well have been present in incipient queen groups. However, division of labor can result in cost skew among group members, and thus, paradoxically, within-group selection may constrain or even reduce specialization. Consistent with this effect, pairs of normally solitary queens were significantly more asymmetrical in their task performance than normally social pairs, in which both queens nearly always performed the behavior to some degree.Communicated by J. Heinze     

Inter-colonial selection for the maintenance of cooperative breeding in the ant Pristomyrmex pungens: a laboratory experiment

The queenless ant Pristomyrmex pungens has an unusual social structure, in which all workers reproduce parthenogenetically and help others. Laboratory experiments manipulating the proportion of post-reproductive foragers in the colony at various rates suggested that colonies with 5–10% forager ratios had the maximum efficiency per-worker. This result suggests that the cooperative colonies may be maintained by colony-level natural selection. Non-cooperative mutants that oviposit but do not forage should increase in relative frequency in the colony in the short term. However, decreased colony productivity and the resulting competition among colonies might eliminate colonies dominated by such mutants in the long term. P. pungens has a viscous population without migration between colonies, which may facilitate this process.     

Neighbours, strangers and male-male aggression as a determinant of lek size

Interactions between males on leks may play an influential role in lek formation and the regulation of lek size. In this paper I present the results of a playback experiment that simulated de novo settlement at sites adjacent to currently existing display territories of the ochre-bellied flycatcher, Mionectes oleagineus. In the study population, males displayed both solitarily and at small leks. A large proportion of males held no display territory at all. A stranger's song was played to both solitary and lekking males from 10 m outside their territorial boundaries. In separate playbacks, lekking males were also played neighbour's song. Both lekking and solitary territorial males reacted to the playback by decreasing their song rate, approaching the playback speaker and, on occasion, attacking the model. Solitarily displaying males responded more aggressively to playback of stranger's song than did lek males. Lek males were able to distinguish between their neighbour's and a stranger's song and did so irrespective of whether it was played from the neighbour's territory or from outside the lek. In addition to distinguishing between neighbours and strangers, lek males modified their responses to these different playbacks depending on where the playback originated. These results suggest that male-male interactions can be influential in structuring leks. In M. oleagineus, interactions between males are aggressive and act to limit rather than augment lek size. Received: 6 March 1996 / Accepted after revision: 9 December 1996     

The Extended Kalman Filter (EKF) as a tool for the assimilation of high frequency water quality data

The Extended Kalman Filter (EKF) was applied to the analysis of high frequency field measurements of dissolved oxygen (DO), water temperature, salinity, collected by multiparametric sensors in the lagoon of Venice. This paper focuses on the practical aspects of the implementation of the EKF as a data assimilation technique and does not deal with the problems associated with the identification of the model. In this regard, the EKF has proved to be a useful tool for the updating of the estimates of the parameters of a simple DO-chlorophyll model, which can be used for linking the high frequency data to meteorological forcings, such as solar radiation and wind, and to other low frequency measurements of water quality parameters, such as the concentrations of Chlorophyll a and nutrients. The model can subsequently be used as a tool for checking the consistency of all this data, and may also be employed for controlling the quality of the data collected by the multiparametric sensors.