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     

Patch departure rules in Bumblebees: evidence of a decremental motivational mechanism

The patch living rules of a pollinator, the bumblebee Bombus terrestris L., are studied here in the framework of motivational models widely used for parasitoids: The rewarding events found during the foraging process are supposed to increase or decrease suddenly the tendency of the insect to stay in the current patch and therefore to adjust the patch residence time to the patch profitability. The foraging behaviour of these pollinators was observed in two environment types to determine their patch-leaving decisions. The rich environment was composed of male-fertile flowers, offering pollen and nectar, and the poor one of male-sterile flowers, offering little nectar and no pollen. The experimental design consisted of a patch system in which inflorescences were evenly arranged in two rows (1 m distance). Residence times of foragers inside inflorescences and rows were analysed by a Cox proportional hazards model, taking into account recent and past experience acquired during the foraging bout. Most of the results showed a decremental motivational mechanism, that is, a reduction in the residence time on the inflorescence or in the row related to exploitation of flowers within inflorescences and inflorescences within rows These results indicate that bumblebees tend to leave the patch using departure rules similar to those found in parasitoids. The results also provide information on the memory, learning and evaluating capabilities of bumblebees especially when rich and poor environments were compared. The patch-leaving mechanism suggested by this study is consistent with the central place foraging theory.     

Does interaction between bumblebees (Bombus ignitus) reduce their foraging area?: bee-removal experiments in a net cage

To examine whether the interaction between bumblebees, Bombus ignitus, reduces their foraging area, we conducted bee-removal experiments in a net cage. In the cage, we set potted Salvia farinacea plants, allowed bumblebees to forage freely on those plants, and followed their plant-to-plant movements to identify a bee with a relatively small foraging area. We then removed all the other foraging bees, except for the bee with a small foraging area, and observed the change of the foraging area of the focal bee under conditions of no interaction with other bees. After the removal of the other bees, all five bees tested enlarged their foraging areas, suggesting that the interaction between bees is an important determinant of their foraging areas. The result also means that bumblebees are able to adjust their foraging areas in response to other foragers, indicating the necessity for future studies to clarify what cues bees use to interact with other bees. Moreover, after the removal treatments, all five bees showed temporary increases in the number of flower probes per plant. This can be explained by their optimal foraging according to the old average intake rate for the plant population and by the delayed changes in response to the new high average energy intake rate after the bee-removal treatments.Communicated by M. Giurfa     

The influence of nectar secretion rates on the responses of bumblebees (Bombus spp.) to previously visited flowers

Bumblebees can avoid recently depleted flowers by responding to repellent scent-marks deposited on flower corollas by previous visitors. It has previously been suggested that avoidance of visited flowers for a fixed period would be a poor strategy, since different plant species vary greatly in the rate at which they replenish floral rewards. In this study, we examined the duration of flower repellency after an initial bumblebee visit, using wild bumblebees (Bombus lapidarius, B. pascuorum and B. terrestris) foraging on four different plant species (Lotus corniculatus, Melilotus officinalis, Phacelia tanacetifolia and Symphytum officinale). We constructed a model to predict flower visitation following an initial visit, based on the nectar secretion pattern of the different plant species, the insect visitation rate per flower, and the search and handling times of bumblebees foraging on the plant species in question. The model predicts an optimal duration of flower avoidance which maximises the rate of reward acquisition for all bees. However, this optimum may be open to cheating. For two plant species, the evolutionary stable strategy (ESS) is a shorter duration of flower avoidance than the optimum. We found the duration of flower avoidance was markedly different among flower species and was inversely related to nectar secretion rates. The predicted ESSs for each plant species were close to those observed, suggesting that the key parameters influencing bumblebee behaviour are those included in the model. We discuss how bees may alter the duration of their response to repellent scents, and other factors that affect flower re-visitation.     

Comparisons of forager distributions from matched honey bee colonies in suburban environments

We conducted experiments designed to examine the distribution of foraging honey bees (Apis mellifera) in suburban environments with rich floras and to compare spatial patterns of foraging sites used by colonies located in the same environment. The patterns we observed in resource visitation suggest a reduced role of the recruitment system as part of the overall colony foraging strategy in habitats with abundant, small patches of flowers. We simultaneously sampled recruitment dances of bees inside observation hives in two colonies over 4 days in Miami, Florida (1989) and from two other colonies over five days in Riverside, California (1991). Information encoded in the dance was used to determine the distance and direction that bees flew from the hive for pollen and nectar and to construct foraging maps for each colony. The foraging maps showed that bees from the two colonies in each location usually foraged at different sites, but occasionally they visited the same patches of flowers. Each colony shifted foraging effort among sites on different days. In both locations, the mean flight distances differed between colonies and among days within colonies. The flight distances observed in our study are generally shorter than those reported in a similar study conducted in a temperate deciduous forest where resources were less dense and floral patches were smaller.     

The communal crop: modulation of sucrose response thresholds of pre-foraging honey bees with incoming nectar quality

We examined whether the quality (concentration) of incoming sucrose solutions returned by foraging honey bees affected the response thresholds of pre-foraging members of the colony. Six pairs of colonies were given ad libitum access to sucrose solution feeders. A colony from each pair was switched from 20–50% sugar concentration feeders while the other continued to have access to 20% sucrose feeders. Proboscis extension response (PER) scores to an increasing series of sucrose concentrations were significantly higher in pre-foragers of colonies foraging on 20% sucrose throughout compared to pre-foragers in colonies where foraging was switched to 50% sucrose. Although all colonies had honey stores, the concentration of sugar solution in non-foraging bees crops were significantly lower in bees from colonies foraging on 20% sucrose compared to those from colonies foraging on 50% sucrose. Because response thresholds to sugar of young bees were modulated by the concentration of sucrose solution returned to colonies, we repeated the 2000 study of Pankiw and Page that potentially confounded baseline response thresholds with modulated scores due to experience in the colony. Here, we examined PER scores to sucrose in bees within 6 h of emergence, prior to feeding experience, and their forage choice 2 to 3 weeks later. Pollen foragers had higher PER scores as newly emerged bees compared to bees that eventually became nectar foragers. These results confirm those of the 2000 study by Pankiw and Page. Combined, these experiments demonstrate that variation in pre-forager sucrose response thresholds are established prior to emerging as adults but may be modulated by incoming resources later on. Whether this modulation has long-term effects on foraging behavior is unknown but modulation has short-term effects and the potential to act as a means of communication among all bees in the colony.Communicated by M. Giurfa     

Effects of parasitic mites and protozoa on the flower constancy and foraging rate of bumble bees

Parasites can affect host behavior in subtle but ecologically important ways. In the laboratory, we conducted experiments to determine whether parasitic infection by the intestinal protozoan Crithidia bombi or the tracheal mite Locustacarus buchneri alters the foraging behavior of the bumble bee Bombus impatiens. Using an array of equally rewarding yellow and blue artificial flowers, we measured the foraging rate (flowers visited per minute, flower handling time, and flight time between flowers) and flower constancy (tendency to sequentially visit flowers of the same type) of bees with varying intensities of infection. Bumble bee workers infected with tracheal mites foraged as rapidly as uninfected workers, but were considerably more constant to a single flower type (yellow or blue). In contrast, workers infected with intestinal protozoa showed similar levels of flower constancy, but visited 12% fewer flowers per minute on average than uninfected bees. By altering the foraging behavior of bees, such parasites may influence interactions between plants and pollinators, as well as the reproductive output of bumble bee colonies. Our study is the first to investigate the effects of parasitic protozoa and tracheal mites on the foraging behavior of bumble bees, and provides the first report of Crithidia bombi in commercial bumble bees in North America.     

Colony energy requirements affect the foraging currency of bumble bees

Summary This study examines whether the foraging behavior of worker bumble bees (Bombus: Apidae) collecting nectar on inflorescences of seablush (Plectritis congesta: Valerianaceae) is affected by colony energetic requirements, which were experimentally manipulated either by adding sucrose solution to honey pots or by removing virtually all available nectar from the pots. The competing hypotheses tested were: (1) no change; energetic requirements do not affect behavior, since there is a single best way to collect food in a given environment; (2) energetic currency; the energetic currency maximized by foragers changes according to colony energetic condition, with nectar-depletion causing a shift from maximizing long-term productivity to maximizing immediate energetic gain, thereby de-emphasizing energetic costs; and (3) predation; foragers devalue risk of predation as risk of starvation increaes, with colony nectar-depletion causing foragers to be less predation riskaverse in order to increase immediate energetic gain. Relative to when their colony energy reserves were enhanced, foragers from nectar-depleted colonies selected smaller inflorescences, visited fewer flowers per inflorescence, probed flowers at a higher rate while on each inflorescence, and walked between inflorescences less often, thereby spending a greater proportion of their foraging trip in flight. These behaviors increased a bee's energetic costs while foraging, and should also have increased its immediate energetic gains, allowing rejection of the no change hypothesis. Predictions of the predation hypothesis were generally not supported, and our results best support the energetic currency hypothesis. Foraging currency of bumble bees therefore appears to be a function of colony energetic state. Offprint requests to: R.V. Cartar     

Trait-mediated effects on flowers: artificial spiders deceive pollinators and decrease plant fitness

Although predators can affect foraging behaviors of floral visitors, rarely is it known if these top-down effects of predators may cascade to plant fitness through trait-mediated interactions. In this study we manipulated artificial crab spiders on flowers of Rubus rosifolius to test the effects of predation risk on flower-visiting insects and strength of trait-mediated indirect effects to plant fitness. In addition, we tested which predator traits (e.g., forelimbs, abdomen) are recognized and avoided by pollinators. Total visitation rate was higher for control flowers than for flowers with an artificial crab spider. In addition, flowers with a sphere (simulating a spider abdomen) were more frequently visited than those with forelimbs or the entire spider model. Furthermore, the presence of artificial spiders decreased individual seed set by 42% and fruit biomass by 50%. Our findings indicate that pollinators, mostly bees, recognize and avoid flowers with predation risk; forelimbs seem to be the predator trait recognized and avoided by hymenopterans. Additionally, predator avoidance by pollinators resulted in pollen limitation, thereby affecting some components of plant fitness (fruit biomass and seed number). Because most pollinator species that recognized predation risk visited many other plant species, trait-mediated indirect effects of spiders cascading down to plant fitness may be a common phenomenon in the Atlantic rainforest ecosystem.     

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     

The choice of two prey types that minimises the probability of starvation

Summary In this paper we investigate the optimal diet of a forager faced with two prey types. Classical optimal foraging theory, based on the maximization of the mean net rate of energetic gain , predicts that the optimal policy is either to take only the more profitable prey type or to take both prey types. The decision between these policies does not depend on the forager's energy reserves or the time available for foraging. We develop two alternative models, based on the minimization of the probability of starvation. In the first model, foraging occurs continuously, and it is optimal to take a prey type if and only if it increases the forager's energy reserves. In the second model foraging stops at dusk, and the forager dies during the night if its reserves at dusk are too low. The optimal policy, which has to be found numerically by dynamic programming, depends on the forager's reserves and the time left till dusk. In general the optimal policy is either to take both types or to take only the more profitable type. Taking both types is optimal when reserves are low, and there is some evidence that this occurs. The models show that factors that have been ignored in classical models may be of importance.     

Traplining by purple-throated carib hummingbirds: behavioral responses to competition and nectar availability

We examined the effects of nectar availability and competition on foraging preferences and revisit intervals of traplining female purple-throated caribs hummingbirds (Eulampis jugularis) to Heliconia patches shared by two individuals or visited solely by one individual. Birds at both shared and solitary patches preferred multiflowered to single-flowered inflorescences, but the magnitude of this preference depended on food availability and competition. During a year of low flower availability, females visited multiflowered inflorescences more frequently than single-flowered inflorescences only when nectar availability was experimentally enhanced; similarly, females at shared patches exhibited a significant preference for multiflowered inflorescences only after experimental increases in nectar availability. Experimental manipulations of nectar availability also had different effects on revisit intervals of birds at shared vs solitary patches. Birds at shared patches responded to patch-wide increases in nectar rewards by increasing the duration of their visit intervals, whereas birds at solitary patches did not. In contrast, birds at solitary patches responded to abrupt losses of nectar at flowers (simulating competition) by decreasing the duration of their visit intervals, whereas a bird at a shared patch did not alter its return interval. The contrasting results between shared vs solitary patches suggest that future studies of traplining behavior should incorporate levels of competition into their design.     

The dynamics of social learning in an insect model,the bumblebee (<Emphasis Type="Italic">Bombus terrestris</Emphasis>)

Bumblebees (Bombus terrestris) are attracted to those particular inflorescences where other bees are already foraging, a process known as local enhancement. Here, we use a quantitative analysis of learning in a foraging task to illustrate that this attraction can lead bees to learn more quickly which flower species are rewarding if they forage in the company of experienced conspecifics. This effect can also be elicited by model bees, rather than live demonstrators. We also show that local enhancement in bumblebees most likely reflects a general attraction to conspecifics that is not limited to a foraging context. Based on the widespread occurrence of both local enhancement and associative learning in the invertebrates, we suggest that social influences on learning in this group may be more common than the current literature would suggest and that invertebrates may provide a useful model for understanding how learning processes based on social information evolve.     

Bee community shifts with landscape context in a tropical countryside.

The ongoing scientific controversy over a putative "global pollination crisis" underscores the lack of understanding of the response of bees (the most important taxon of pollinators) to ongoing global land-use changes. We studied the effects of distance to forest, tree management, and floral resources on bee communities in pastures (the dominant land-use type) in southern Costa Rica. Over two years, we sampled bees and floral resources in 21 pastures at three distance classes from a large (approximately 230-ha) forest patch and of three common types: open pasture; pasture with remnant trees; and pasture with live fences. We found no consistent differences in bee diversity or abundance with respect to pasture management or floral resources. Bee community composition, however, was strikingly different at forest edges as compared to deforested countryside only a few hundred meters from forest. At forest edges, native social stingless bees (Apidae: Meliponini) comprised approximately 50% of the individuals sampled, while the alien honeybee Apis mellifera made up only approximately 5%. Away from forests, meliponines dropped to approximately 20% of sampled bees, whereas Apis increased to approximately 45%. Meliponine bees were also more speciose at forest edge sites than at a distance from forest, their abundance decreased with continuous distance to the nearest forest patch, and their species richness was correlated with the proportion of forest cover surrounding sample sites at scales from 200 to 1200 m. Meliponines and Apis together comprise the eusocial bee fauna of the study area and are unique in quickly recruiting foragers to high-quality resources. The diverse assemblage of native meliponine bees covers a wide range of body sizes and flower foraging behavior not found in Apis, and populations of many bee species (including Apis), are known to fluctuate considerably from year to year. Thus, the forest-related changes in eusocial bee communities we found may have important implications for: (1) sustaining a diverse bee fauna in tropical countryside; (2) ensuring the effective pollination of a diverse native plant community; and (3) the efficiency and stability of agricultural pollination, particularly for short-time-scale, mass-flowering crops such as coffee.     

The importance of handling time for the flight directionality in bees

Summary Individual workers of the honeybee (Apis mellifera), trained to collect food from a patch of artificial flowers, were used to test the following hypotheses about the mechanism leading to a decrease in flight directionality when moving from one flower to the next. Directionality decreases with (1) an increasing amount of energy taken from a flower, (2) an increasing amount of time spent on a flower, or (3) an increasing profitability of the flower, i.e. rate of nectar uptake. The bees were tested singly on an arrangement with equidistant flowers. They could move from a decision point forward, right, left, or backwards to the next flower. The rewards at the decision point were altered. When rewards at this point were compared that offered the same quality of nectar (50% sugar solution), the time hypothesis (2) was consistent with the observed behaviour of the bees. When conditions were compared that involved two different reward qualities (50% and 25% sugar solation), none of the original hypotheses could entirely account for the results.It is suggested that a slight modification of the time hypothesis would be consistent with the observations: The bees might possibly forget their arrival direction on the flower with increasing time, but forgetting the direction of the last flower visited is intensified with more concentrated rewards.     

Lévy flight patterns are predicted to be an emergent property of a bumblebees’ foraging strategy

Bumblebees forage uninterrupted for long periods of time because they are not distracted by sex or territorial defense and have few predators. This has led to a long running debate about whether bumblebees forage optimally. This debate has been enriched by the possibility that bumblebees foraging within clover patches have flight patterns that can be approximated by Lévy flights. Such flight patterns optimise the success of random searches. Bumblebees foraging within a flower patch tend to approach the nearest flower but then often depart without landing or probing it if it has been visited previously; unvisited flowers are not rejected in this manner. Here, this foraging behaviour has been replicated in numerical simulations. Lévy flight patterns are found to be an inconsequential emergent property of a bumblebees’ foraging behaviour. Lévy flights are predicted to emerge when bees reject at least 99% of previously visited flowers. A foraging bumblebee can certainly empty a clover flower head of nectar in one visit, but lower rates of rejection are observed for many other flowers. These findings suggest that Lévy flight patterns in foraging bumblebees are rare and specific to a few flower species and that if they exist, then they are not part of an innate, evolved optimal searching strategy.     

Why are bumble bees risk-sensitive foragers?

Summary In a controlled laboratory experiment, we re-examined the question of bumble bee risk-sensitivity. Harder and Real's (1987) analysis of previous work on bumble bee risk aversion suggests that risk-sensitivity in these organisms is a result of their maximizing the net rate of energy return (calculated as the average of expected per flower rates). Whether bees are risk-sensitive foragers with respect to minimizing the probability of energetic shortfall is therefore still an open question. We examined how the foraging preferences of bumble bees for nectar reward variation were affected by colony energy reserves, which we manipulated by draining or adding sucrose solution to colony honey pots. Nine workers from four confined colonies of Bombus occidentalis foraged for sucrose solution in two patches of artificial flowers. These patches yielded the same expected rate of net energy intake, but floral volumes were variable in one patch and constant in the other. Our results show that bumble bees can be both risk-averse (preferring constant flowers) and risk-prone (preferring variable flowers), depending on the status of their colony energy reserves. Diet choice in bumble bees appears to be sensitive to the target value a colony-level energetic requirement. Offprint requests to: R.V. Cartar     

Colour-independent shape recognition of cryptic predators by bumblebees

Predators hunting for cryptic prey use search images, but how do prey search for cryptic predators? We address this question using the interaction between bumblebees and the colour-changing crab spider Misumena vatia which can camouflage itself on some flowers. In laboratory experiments, we exposed bumblebees to an array of flowers concealing robotic predators (a trapping mechanism combined with a 3D life-sized model of a crab spider or a circle). Groups of bees were trained to avoid either cryptic yellow spiders or yellow circles (equal area to the spiders) or remained predator naive. The bees were then exposed to a new patch of white flowers containing some cryptic predators (either white spiders, white circles or a mixture of both). We monitored individual foraging choices and used a 3D video tracking system to quantify the bees’ flight behaviour. The bees trained to avoid cryptic spiders, chose 40% fewer spider-harbouring flowers than expected by chance, but were indifferent to cryptic circles. They also aborted a higher proportion of landings on flowers harbouring spiders, ultimately feeding from half as many ‘dangerous’ flowers as naive bees. Previous encounters with cryptic spiders also influenced the flight behaviour of bees in the new flower patch. Experienced bees spent more time inspecting the flowers they chose to reject (both with and without concealed spiders) and scanned from side to side more in front of the flowers to facilitate predator detection. We conclude that bees disentangle shape from colour cues and thus can form a generalised search image for spider shapes, independent of colour.     

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

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

The establishment of foraging flocks in house sparrows: risk of predation and daily temperature

Summary The foraging decisions of animals often reflect a trade-off between the risk of predation and efficient foraging. One way an animal may reduce the risk of predation, and hence exploit a resource patch in relative safety, is by foraging in a group. Solitary pioneer sparrows often recruit others to a food source by making chirrup calls in order to establish foraging flocks. This study describes the decisions of house sparrows that arrive at food resources of different risks of predation. Four feeding sites at different distances from a perching site and from an observer were presented to sparrows. When the feeder was adjacent to the perching site and far from the observer, the pioneers chirruped less frequently and were more likely to forage alone than when the feeder was in the other three positions. There were differences in the scanning behaviour of sparrows at these sites, suggesting that they were responding to different risks of predation. Furthermore, the chirrup rates of pioneer sparrows in this study and a previous study were found to be negatively correlated with maximum daily temperature. This is consistent with the hypothesis that energy requirements may affect the flock establishment decisions of sparrows, and that the benefits of foraging in flocks may be greater at lower temperatures.