Experimental analysis of worker division of labor in bumblebee nest thermoregulation (<Emphasis Type="Italic">Bombus huntii</Emphasis>, Hymenoptera: Apidae)

Bumblebee colonies experience daily and seasonal fluctuations in ambient temperature, but proper brood development requires a stable nest temperature. This study examined how adaptive colony responses to changing ambient temperature are achieved through the in-nest workers’ behavioral plasticity. We studied three Bombus huntii colonies in the laboratory. In the first experiment, we manipulated ambient temperature and recorded brood cell incubation and wing fanning by individually marked, known-age bees. The colonies maintained their nests closer to appropriate brood development temperatures (28 to 32°C) when exposed to a range of ambient temperatures from 10.3 to 38.6°C. Incubation activity was greater in cooler treatment conditions, whereas in the highest temperature treatment, some bees fanned and others moved off the brood. As the ambient temperature dropped, workers increased the duration of their incubating bouts, but, except at the highest temperature, the number of workers that incubated did not differ significantly among treatments. A subset of the bees incubated significantly more than their nest mates, some of which never incubated. Worker body size, but not age, was a good predictor of incubation rates, and smaller bees incubated at higher rates. In the second experiment, we removed the most actively incubating workers. Immediately after removals, the total colony incubation effort was lower than pre-removal levels, but incubation effort rebounded toward pre-removal levels after 24 h. The increased thermoregulatory demand after removals was met primarily by bees increasing their rates of incubation rather than by bees switching from a different task to incubation. We conclude that some B. huntii workers specialize on nest thermoregulation, and that changes in work rates are more important than task switching in meeting thermal challenges.     

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.     

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     

Regulation of worker reproduction in bumblebees (Bombus terrestris): workers eavesdrop on a queen signal

In the annual bumblebee Bombus terrestris, the onset of queen-worker conflict over male production is seasonally and socially constrained. Workers will do better if they start to reproduce (the so-called competition phase) only after ascertaining that larvae are committed to gyne development but before the season ends because they gain more by rearing sister-gynes than their own sons. Here, we tested two nonmutually exclusive hypotheses as to what triggers the onset of worker reproduction: Workers can directly monitor larval development and/or workers eavesdrop on the queen signal that directs gyne development. Exposing workers to gyne larvae through a double mesh did not advance the competition phase compared to control colonies. However, when workers, but not the queen, were allowed contact with gyne larvae, both the competition phase and gyne production were advanced. Thus, while larvae do not emit a volatile pheromone that discloses their developmental route, the physical contact of workers with such larvae triggers early competition phase. However, workers exclusively exposed to worker larvae (colonies prevented from producing gyne larvae) started to reproduce at the same time as control colonies. Replacing the resident queen with an older queen (from gyne-rearing colonies) advanced the competition phase, irrespective of worker age. The results are consistent with the hypothesis that workers eavesdrop on the queen pheromones. This is adaptive because it allows workers a broader time-window for reproduction and thus to gain fitness from rearing both sister-gynes and sons before the season ends without affecting colony development.     

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.     

Worker reproduction in the ponerine ant Ophthalmopone berthoudi: an alternative form of eusocial organization

Summary Colonies of the ponerine Ophthalmopone berthoudi were collected throughout the year. The queen caste is absent. Dissection of large numbers of workers revealed that many of them (up to 100 in one nest) are inseminated and produce eggs. The ovaries are small and contain very few mature oocytes, indicating that there is a slow rate of egg-laying. Workers are produced throughout the year, and all are capable of becoming functional reproductives. However, only those that are sexually-attractive during the limited period of male activity become mated. Thus the percentages of mated laying workers (=gamergates) fluctuate seasonally (Fig. 2). Successive generations of gamergates do not overlap. Observation of nests in the field and in the laboratory indicated that gamergates were never active above ground. There is no aggression between them, and their numbers are not socially regulated. There are few interactions between gamergates and non-reproductive workers, and the former do not acquire more food during termite meals. The notion of parental oppression is undermined by the complete loss of the meen caste, while the nature of the breeding system of this ant leads to the prediction of low relatedness between nestmates.     

The social behavior of Leptothorax allardycei (Hymenoptera,Formicidae): time budgets and the evolution of worker reproduction

Summary The use of time by workers of the ant Leptothorax allardycei (Mann) is examined. Theoretical predictions are developed concerning the maximal lowering in colony reproductive output that is consistent with the evolution of worker production. Measurements are made of the effect of aggression on colony efficiency. Analysis of time budgets indicate that a typical ant spends a large fraction (0.55) of its time quiescent and another large fraction of time (0.32) involved in undifferentiated activity. Dominance activity and brood care together make up about 11% of the total time. The amount of time spent on dominance activity is negatively related to the amount of time spent on brood care, but positively related to the amount of time that an ant is active. The amount of time that an ant has available for brood care which is actually spent on brood care declines with the amount of time spent on dominance activity. The amount of time that a worker spends feeding liquid food to larvae is a function of hierarchy rank; alpha spends the most time, beta less and gamma still less. The spread of the trait of worker reproduction is examined theoretically, with particular regard to the associated costs to colony reproduction. Worker reproduction can spread through a population, under a variety of formulations, provided the cost to colony reproduction is less than some critical value in the neighborhood of 0.17–0.22 of the total colony output. The cost of worker reproduction in L. allardycei is estimated in two ways: as a time cost and as a reduction in the total number of brood tended per unit time. The two estimates of cost are 0.15 and 0.13 respectively. The reproductive options of the worker caste and the division of reproductive labor vary considerably between species. Reproduction by workers yields fitness differences between workers and results in competition among workers with the result that colony efficiency is affected.     

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.     

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.     

Social organization and division of labour in colonies of the polistine wasp,Belonogaster petiolata

Summary Foundresses in pre-emergence and post-emergence nests of Belonogaster petiolata were organized into linear dominance hierarchies according to their level of physical aggression towards cofoundresses. The female at the top of the hierarchy became the queen, while foundresses ranked below her became worker-like subordinates. In pre-matrifilial colonies, worker offspring were socially subordinate to both their queen and the subordinate foundresses. Queens of matrifilial colonies retained full social dominance over their workers. Queens were reproductively dominant over subordinates and workers, and laid the majority of, if not all, surviving eggs. Subordinate-laid eggs were invariably discovered and destroyed by the queen through oophagy; workers in pre-matrifilial and matrifilial colonies never laid or ate eggs. Colonies contained a single (and the same) functional queen throughout the pre- and post-emergence periods and were, therefore, long-term monogynous.In both established pre-emergence colonies and post-emergence colonies, virtually all foraging for food and nesting material was performed by the subordinates and workers. More dominant subordinates generally foraged less than low-ranked subordinates. Queens were more active builders than subordinates or workers in pre-matrifilial and matrifilial colonies. Queens enjoyed a surplus in exchanged food loads, while subordinates and workers did not. Among cofoundresses, an advantage in food exchange was also positively associated with dominance rank. Queens solicited larvae for their salivary fluid more often than did subordinates and workers. Among cofoundresses, frequency of adult-larva trophallaxis was positively associated with rank. Queens rested most often in the central zones of the nest containing late instar larvae and pupae, while subordinates and particularly workers spent more time in the peripheral, broodless regions of the nest.This paper is dedicated to the late Professor Leo Pardi, whose pioneering studies of Belonogaster served as a constant source of inspiration and reference for the present work     

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.     

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.     

Locomotor impairment and defense in gravid lizards (Eumeces laticeps): behavioral shift in activity may offset costs of reproduction in an active forager

Summary Female Eumeces laticeps experience a substantial decrease in running speed (ca. 25%) and an even greater loss of endurance (slightly over 50%) while gravid. Because some widely foraging lizards, including E. laticeps, rely primarily on running to escape predators, the decreases in speed and stamina may contribute to an increased risk of predation. However, observations suggest that gravid females become less active or conspicuous on the surface. Ambush foraging lizards rely relatively more on crypsis associated with immobility to avoid predation and thus can have greater average relative clutch mass (RCM) than active foragers. Behavioral compensation for locomotor impairment by becoming less active or conspicuous may allow some species the advantages inherent in both high relative clutch mass when gravid and the increased energetic profitability of active foraging when not gravid. As females gain weight during the breeding season, they may forage actively until the risk due to increasing locomotor impairment becomes too great and then change defensive strategy to greater reliance on crypsis. Without such a shift, widely foraging squamate reptiles may be less able than ambush foragers to exploit life-historical strategies demanding high current investment in reproduction.     

Parasitic flies (Diptera: Phoridae) influence foraging rhythms and caste division of labor in the leaf-cutter ant,Atta cephalotes (Hymenoptera: Formicidae)

Summary Three lines of evidence, including interspecific comparisons, temporal division of foraging between size castes, and experimental manipulations, suggest that the diurnal parasitoid Neodohrniphora curvinervis (Diptera: Phoridae) influences both the caste sizes and numbers of leaf-cutter ants (Atta cephalotes) that leave their underground nests to collect leaves. At Parque Nacional Corcovado in Costa Rica, A. cephalotes was attacked by Neodohrniphora during the daytime, and foraged less during the day than at night; a closely related ant at the same site, A. colombica, had no phorid parasites and foraged exclusively during the day. Most daytime foragers of A. cephalotes were smaller than the lower size threshold for attack by Neodohrniphora, while nocturnal foragers, active when parasitoids were absent, were both larger than this threshold and within the energetically optimal size range for foraging. When I supplied artificial lighting to allow phorids to hunt at A. cephalotes colonies past dusk, ants foraged less than when light was provided but flies were removed. The influence of Neodohrniphora on the foraging activity of A. cephalotes may explain why investigations focusing on abiotic factors have largely failed to discover what drives this ant's daily foraging cycles, and suggests that forager sizes are influenced not only by energetic efficiency, but also by the threat of parasitism.     

Insect herbivory may cause changes in the visual properties of leaves and affect the camouflage of herbivores to avian predators

Behavioral Ecology and Sociobiology - An individual’s metabolic competence is important when escalating to costly behaviours in agonistic encounters. The use of broken shells in the wild...     

A study of reproduction and other life cycle phenomena in planktonic protists using an acridine orange fluorescence technique

The percentage of dividing individuals and temporal reproductive patterns were determined for natural populations of several planktonic protists including five species of tintinnids, a dinoflagellate, and a diatom. To obtain these data, a method was used in which the nuclei of planktonic ciliates and phytoplankters can be fluorescently stained with acridine orange at the time of collection and fixation. The technique is simple and can be used routinely in studies of reproduction or other life cycle phenomena of natural protistan populations. For the tintinnids, often more than half of the individuals were in some recognizable stage of fission; periodicity in the division process was only observed once and apparently followed a pulse of conjugation in the population. With the diatom Ditylum brightwellii the fluorescent staining technique yielded data on the extent and timing of division which were consistent with, but more complete than, previous enumerations of paired cells.The support of the National Science Foundation (OCE-7819566) is acknowledged     

Quantitative variation in ecological and hormonal variables correlates with spatial organization of pronghorn (Antilocapra americana) males

Whereas variation in pronghorn (Antilocapra americana) spatial organization is well documented, underlying ecological or physiological explanations are not well understood. This study quantitatively describes spacing systems of pronghorn males and correlates of their spatial organization. I collected behavioral data from two populations in South Dakota (Wind Cave) and Montana (Bar Diamond) to determine if males differed in space use, response to intruders, and behavior patterns indicative of area defense. I measured sex ratio and population density, and I examined characteristics of food resources, including forb species diversity, richness, coverage, biomass, and nitrogen content, and how they changed during the growing season. I also collected and analyzed fecal samples to determine if males differed in testosterone concentrations. Pronghorn males at Wind Cave were more territorial than males at Bar Diamond, although males at Bar Diamond became more territorial during the second year. The forb community at Wind Cave was more diverse, contained greater amounts of forbs later in summer, and had a higher nitrogen content later in summer. Population density was lower at Wind Cave, although density dropped at Bar Diamond during the second year, and sex ratios were skewed toward males at Bar Diamond. Finally, males at Wind Cave had higher testosterone concentrations than did Bar Diamond males, although differences were not statistically significant. With lower population density and higher forb abundance and quality, food resources were more economically defensible at Wind Cave, and males were more territorial there. Analyses using these and other pronghorn populations revealed that population density and sex ratio correlated weakly with spatial organization, whereas precipitation correlated most strongly, which suggests plant productivity has a powerful role in determining pronghorn territoriality. Received: 16 June 1999 / Received in revised form: 21 September 1999 / Accepted: 31 December 1999     

Reproductive conflict in honey bees: a stalemate of worker egg-laying and policing

 Using electrophoretic markers, eggs laid by workers were identified in honey bee (Apis mellifera) colonies with a queen. Based on extrapolation, these represented about 7% of the unfertilized (male) eggs laid in the colonies. A very small proportion of workers (of the order of 0.01%) lay these eggs. Worker-laid eggs are rapidly removed, so that very few sons of workers are reared. Thus the reproductive cooperation in bee colonies is maintained by ongoing antagonistic interactions among the members of the colony, with worker laying and egg removal policing by other workers being relatively common. Received: 24 November 1995/Accepted after revision: 25 May 1996