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

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

Tactile learning in resin foraging honeybees

Honeybees harvest and use plant resins in a mixture called propolis to seal cracks and smooth surfaces in the nest architecture. Resins in the nest may be important in maintaining a healthy colony due to their antimicrobial properties. This study had two main objectives: (1) Provide initial insight on the learning capabilities of resin foraging honeybees; (2) analyze the sensitivity of resin foraging honeybees to tactile stimuli to elucidate its possible role as a mechanism behind resin foraging. The first objective provides insight into the phenotype of these bees as compared to other forager types, while the second creates a starting point for further work on behavioral mechanisms of resin foraging. Using tactile proboscis extension response conditioning, we found that resin foragers learned to associate two different tactile stimuli, the presence of a gap between two plates and a rough sandpaper surface, with a sucrose reward significantly better than pollen foragers. The results of differential tactile conditioning exhibited no significant difference in the ability of resin foragers to discriminate between smooth and rough surfaces as compared to pollen foragers. We also determined that the sucrose response thresholds (SRTs) of returning resin foragers were lower compared to returning pollen foragers, but both resin foragers and pollen foragers learned a floral odor equally well. This is the first study to examine SRTs and conditioning to tactile and olfactory stimuli with resin foraging honeybees. The results provide new information and identify areas for future research on resin collectors, an understudied foraging phenotype.     

Memory dynamics and foraging strategies of honeybees

Summary The foraging behavior of a single bee in a patch of four electronic flower dummies (feeders) was studied with the aim of analyzing the informational components in the choice process. In different experimental combinations of reward rates, color marks, odors and distances of the feeders, the behavior of the test bee was monitored by a computer in real time by several devices installed in each feeder. The test bee optimizes by partially matching its choice behavior to the reward rates of the feeders. The matching behavior differs strongly between stay flights (the bee chooses the feeder just visited) and shift flights (the bee chooses one of the three alternative feeders). The probability of stay and shift flights depends on the reward sequence and on the time interval between successive visits. Since functions describing the rising probability of stay flights with rising amounts of sucrose solution just experienced differ for the four feeders, it is concluded that bees develop feeder-specific memories. The choice profiles of shift flights between the three alternative feeders depend on the mean reward rate of the feeder last visited. Good matching is found after visits to the low-reward feeders and poor matching following departure from the high-reward feeders. These results indicate that bees use two different kinds of memories to guide their choice behavior: a transient short-term working memory that is not feeder-specific, and a feeder-specific long-term reference memory. Model calculations were carried out to test this hypothesis. The model was based on a learning rule (the difference rule) developed by Rescorla and Wagner (1972), which was extended to the two forms of memories to predict this operant behavior. The experiments show that a foraging honeybee learns the properties of a food source (its signals and rewards) so effectively that specific expectations guide the choice behavior. Correspondence to: R. Menzel     

Group foraging, patch exploitation time and the finder's advantage

 We use a combination of the marginal value theorem (MVT) of Charnov (1976), and a group foraging model featuring information sharing to address patch residence in an environment where food occurs in discrete patches. We shall show that among equal competitors the optimal patch time for the individual that finds the food patch is shorter than that for the non-finder among equal competitors, T _E < T _N. This is the case if the patch-finder commences food harvesting in the patch earlier and manages to monopolise a fraction of the prey items (finder's advantage) before the other individuals come to take their benefit. When individuals differ in their food-searching abilities so that some of them (producers) contribute proportionally more to food-searching than others (scroungers), and differ in ability to compete for the food found, a difference emerges between producer and scrounger individuals in the optimal patch time. Within a patch we always have the finder's advantage (T _E < T _N) regardless of phenotype. Between patches a suite of optimal patch times for encountering individuals emerges depending on the performance of producers and scroungers when changing from solitary feeding to feeding in a group. The optimal patch time for individuals that are affected more severely by competition is shorter than that for individuals of the phenotype with better competitive ability. When both phenotypes are affected similarly no difference in optimal patch times emerges. Received: 13 February 1996 / Accepted after revision: 28 September 1996     

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.     

Effects of interactions among genotypically diverse nestmates on task specialization by foraging honey bees (Apis mellifera)

Summary Recent studies have shown that differences in patterns of task specialization among nestmate honeybee workers (Apis mellifera) can be explained, in part, as a consequence of genotypic variability. Here, we present evidence supporting the hypothesis that an individual's pattern of task specialization is affected not only by her own genotype, but, indirectly, by the genotypes of her nestmates. Workers from two strains of honey bees, one selected for high pollen hoarding, the other for low pollen hoarding, were observed in colonies of their respective parent strains and in colonies of the other strain. Worker genotype and host-colony type affected foraging activity. Workers from the high strain fostered in low-strain colonies returned with pollen on 75.6% of total foraging trips, while workers from the high strain fostered in high-strain colonies returned with pollen on 53.5% of total trips. Workers from the low strain fostered in low-strain colonies returned with pollen on 34.8% of total foraging trips while workers from the low strain fostered in high-strain colonies returned with pollen on 2.6% of total trips. Similar results were obtained in a second experiment. We suggest that workers influence the behavior of their nestmates indirectly through their effects on the shared colony environment. The asymmetry seen in the response of workers from these strains to the two types of colony environments also suggests that these genotypes exhibit different norms of reaction. Offprint requests to: N.W. Calderone     

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     

Individual energetic state can prevail over social regulation of foraging in honeybees

The energetic state of an individual is a fundamental driver of its behavior. However, an individual in a eusocial group such as the honeybees is subject to the influence of both the individual and the colony energetic states. As these two states are normally coupled, it has led to the predominant view that behaviors, such as foraging, are dictated by the colony state acting through social regulatory mechanisms. Uncoupling the energetic state of an individual honeybee from its colony by feeding it with a non-nutritious sugar, we show that energetically stressed bees in a colony with full food stores do not consume this food to meet their energetic shortfall but instead compensate by first reducing their activity level and then by increasing their foraging rate. This suggests that foraging in eusocial groups is still partly under the regulatory control of the energetic state of the individual and supports the notion that regulatory mechanisms in solitary insects have been co-opted to drive altruistic behavior in eusocial insects. The observation that energetically stressed bees also experience higher mortality during foraging also suggests that energetic stress mediated by a variety of factors can be a common mechanism that underlies the recent observation of bees disappearing from their colonies. We also discuss how nutritional imbalance in a social insect individual can alter its behavior to influence colony life history.     

Habitat specialization and the exploitation of allochthonous carbon by zooplankton

The significance of spatial subsidies depends on consumer resource interactions in the recipient habitat. Lakes are subsidized by terrestrial carbon sources, but the pathways of allochthonous carbon through lake food webs are complex and not well understood. Zooplankton vertically partition resources within stratified lakes in response to life history trade-offs that are governed by predators, the quantity and quality of food, and abiotic conditions (e.g., UV, temperature, and viscosity). We measured habitat specialization of zooplankton in an oligotrophic lake where allochthonous and autochthonous resources varied with depth. During stratification, the quantity and quality of zooplankton food was highest in the hypolimnion. We used a yearlong time series of the delta13C of zooplankton and particulate organic matter (POM) to determine which zooplankton species exploited hypolimnetic rather than epilimnetic resources. Because the delta13C of POM decreased with depth, we used the delta13C of zooplankton to detect inter- and intraspecific variation in habitat selection. We incubated Daphnia pulex at discrete depths in the water column to confirm that the delta13C of zooplankton can indicate habitat specialization. Zooplankton that specialized in the epilimnion relied more on allochthonous carbon sources than those that specialized in the hypolimnion. Therefore, the fate of allochthonous carbon subsidies to lakes depends on spatially explicit consumer-resource interactions.     

Nectar-receiver behavior in relation to the reward rate experienced by foraging honeybees

Since forager honeybees change their food-unloading behavior according to nectar-source profitability, an experiment was performed in order to analyze whether food-receivers modify their within-hive tasks related to different reward conditions. We offered individual foragers two reward conditions at a rate feeder while an additional feeder offered a constant reward and was of free access to the rest of the hive. Both feeders were the only food sources exploited by the colony during the assays since a flight chamber was used. After receiving nectar, hive bees performed processing cycles that involved several behaviors and concluded when they returned to the delivery area to receive a new food sample. During these cycles, receivers mainly performed oral contacts offering food, or inspected cells, and often both. In the latter case, both behaviors occurred simultaneously and at the same distance from the hive entrance. When they performed a single task, either the occurrence of cell inspections increased or contact offerings decreased for the highest reward rate offered to the donor-forager. Receivers also begged for food more often after interacting with low-profit foragers. Thus, the profitability of the food source exploited by nectar-forager honeybees could affect receiver behaviors within the hives based on individual-to-individual interactions.Communicated by R.F.A. Moritz     

On comparing monopoly and competition in exhaustible resource exploitation

It is widely believed that exhaustible resource monopolies do not enjoy as much market power as standard non-resource monopolies, and may even produce in a socially optimal way. We argue that this paradoxical result arises from an inappropriate comparison methodology. When similar assumptions are applied to the resource, and the conventional cases, we show that the resource monopoly behaves as expected, i.e., restricts supply.     

Sensori-motor learning and its relevance for task specialization in bumble bees

Individual bees often restrict their visits to only a few species out of the multitude of available plants. This flower constancy is likely caused by limitations of memory for motor patterns, sensory stimuli, or reward levels. Here we test the implications of sensori-motor learning and memory for flower constancy. Artificial “flowers” with two distinct “morphologies” were used, so that in each flower type, a different motor pattern was needed to reach the nectar. As in natural flowers, these morphological types were associated with sensory signals (blue and yellow color stimuli). Bees which learned only a single task were more efficient in several ways than those which had learned two: they made fewer errors, had shorter flower handling times, took shorter times to correct errors, and transitions between flowers were initially more rapid. For bees which had learned two tasks, performance depended strongly on the training schedule: if each task was learned with blocked trials, the memory for the second appeared to interfere with that for the first. Interference affected only the association between flower signal and motor pattern, not the motor pattern itself. This was not the case if bees were trained for both tasks with alternating trials. In that case, bees rapidly learned both tasks, albeit with worse saturation levels than bees which had learned only one. Bees transferred the experience gained on one task to a second task: their initial performance on the second task was better than their initial performance on the first. On the other hand, performance on the second task in the saturation level (in which bees no longer improve their efficiency) was worse than on the first task (negative transfer). In the saturation phase, performance did not directly depend on switch frequency, but on whether the bee had one or two options in memory. Thus, while bees would become proficient at two tasks more quickly if their acquisition phase included switches, such switches had no measurable effect in the saturation phase. The implications of these findings for foraging are discussed using modern learning theory. Received: 4 April 1997 / Accepted after revision: 8 August 1997     

The influence of pollen quality on foraging behavior in honeybees (Apis mellifera L.)

Individual and colony-level foraging behaviors were evaluated in response to changes in the quantity or nutritional quality of pollen stored within honeybee (Apis mellifera L.) colonies. Colonies were housed in vertical, three-frame observation hives situated inside a building, with entrances leading to the exterior. Before receiving treatments, all colonies were deprived of pollen for 5 days and pollen foragers were marked. In one treatment group, colony pollen reserves were quantitatively manipulated to a low or high level, either by starving colonies of pollen or by providing them with a fully provisioned frame of pollen composed of mixed species. In another treatment group, pollen reserves were qualitatively manipulated by removing pollen stores from colonies and replacing them with low- or high-protein pollen supplements. After applying treatments, foraging rates were measured four times per day and pollen pellets were collected from experienced and inexperienced foragers to determine their weight, species composition, and protein content. Honeybee colonies responded to decreases in the quantity or quality of pollen reserves by increasing the proportion of pollen foragers in their foraging populations, without increasing the overall foraging rate. Manipulation of pollen stores had no effect on the breadth of floral species collected by colonies, or their preferences for the size or protein content of pollen grains. In addition, treatments had no effect on the weight of pollen loads collected by individual foragers or the number of floral species collected per foraging trip. However, significant changes in foraging behavior were detected in relation to the experience level of foragers. Irrespective of treatment group, inexperienced foragers exerted greater effort by collecting heavier pollen loads and also sampled their floral environment more extensively than experienced foragers. Overall, our results indicate that honeybees respond to deficiencies in the quantity or quality of their pollen reserves by increasing the gross amount of pollen returned to the colony, rather than by specializing in collecting pollen with a greater protein content. Individual pollen foragers appear to be insensitive to the quality of pollen they collect, indicating that colony-level feedback is necessary to regulate the flow of protein to and within the colony. Colonies may respond to changes in the quality of their pollen stores by adjusting the numbers of inexperienced to experienced foragers within their foraging populations.     

太湖流域湖泊滩地资源及其开发利用

在调查和分析太湖流域湖泊滩地资源特征和开发利用状况的基础上,着重探讨了滩地围垦对流域生态环境的影响,并提出今后开发利用滩地资源的方向和对策。     

On the integration of individual foraging strategies with colony ergonomics in social insects: nectar-collection in honeybees

Summary We experimentally tested whether foraging strategies of nectar-collecting workers of the honeybee (Apis mellifera) vary with colony state. In particular, we tested the prediction that bees from small, fast growing colonies should adopt higher workloads than those from large, mature colonies. Queenright small colonies were set up by assembling 10 000 worker bees with approximately 4100 brood cells. Queenright large colonies contained 35 000 bees and some 14 500 brood cells. Thus, treatments differed in colony size but not in worker/brood ratios. Differences in workload were tested in the context of single foraging cycles. Individuals could forage on a patch of artificial flowers offering given quantities and qualities of nectar rewards. Workers of small colonies took significantly less nectar in an average foraging excursion (small: 40.1 ± 1.1 SE flowers; large: 44.8 ± 1.1), but spent significantly more time handling a flower (small: 7.3 ± 0.4 s ; large: 5.8 ± 0.4 s). When the energy budgets for an average foraging trip were calculated, individuals from all colonies showed a behavior close to maximization of net energetic efficiency (i.e., the ratio of net energetic gains to energetic costs). However, bees from small colonies, while incurring only marginally smaller costs, gained less net energy per foraging trip than those from large colonies, primarily as a result of prolonged handling times. The differences between treatments were largest during the initial phases of the experimental period when also colony development was maximally different. Our results are at variance with simple models that assume natural selection to have shaped behavior in a single foraging trip only so as to maximize colony growth. Offprint requests to: P. Schmid-Hempel     

Interannual variability of growth and reproduction in Bursera simaruba: the role of allometry and resource variability

Plants are expected to differentially allocate resources to reproduction, growth, and survival in order to maximize overall fitness. Life history theory predicts that the allocation of resources to reproduction should occur at the expense of vegetative growth. Although it is known that both organism size and resource availability can influence life history traits, few studies have addressed how size dependencies of growth and reproduction and variation in resource supply jointly affect the coupling between growth and reproduction. In order to understand the relationship between growth and reproduction in the context of resource variability, we utilize a long-term observational data set consisting of 670 individual trees over a 10-year period within a local population of Bursera simaruba (L.) Sarg. We (1) quantify the functional form and variability in the growth-reproduction relationship at the population and individual-tree level and (2) develop a theoretical framework to understand the allometric dependence of growth and reproduction. Our findings suggest that the differential responses of allometric growth and reproduction to resource availability, both between years and between microsites, underlie the apparent relationship between growth and reproduction. Finally, we offer an alternative approach for quantifying the relationship between growth and reproduction that accounts for variation in allometries.     

Defense by exploitation in the Florida carpenter ant, Camponotus floridanus, at an extrafloral nectar resource

When resources in a territory have a patchy distribution, intruders may successfully exploit unguarded patches. In such cases, territory owners may use exploitative strategies to reduce the gains of the intruders. The territorial ant Camponotus floridanus attends the leaf nectaries of Urena lobata, which are also visited by the ant Pseudomyrmex mexicanus and other intruders. Residents visited the nectaries at a high rate and in a systematic way, and thereby depressed the mean standing crop per nectary. This reduces the gains of randomly visiting intruders which obtain the mean standing crop per nectary visit. Two or three residents were present on large plants and kept the mean standing crop at the same low level as at small plants with a single ant. This is an ideal free distribution of the ants. The resident ants visited the nectaries at a rate which increased in proportion to the nectar production per nectary. This is the expected systematic visitation when nectar production varies between nectaries. It is suggested that systematic visitation and maximization of the visitation rate are evolutionarily stable strategies in both residents and intruders. However, the intruders are constrained by the residents, so that they visit the nectaries less frequently and in a random manner, and thus have a lower gain rate. When the resident was temporarily absent, the intruders visited the nectaries at a high rate and systematically. Received: 31 May 1999 / Received in revised form: 15 November 1999 / Accepted: 6 December 1999