Choosing rewarding flowers; perceptual limitations and innate preferences influence decision making in bumblebees and honeybees

Flowers exhibit great intra-specific variation in the rewards they offer. At any one time, a significant proportion of flowers often contain little or no reward. Hence, foraging profitably for floral rewards is problematic and any ability to discriminate between flowers and avoid those that are less rewarding will confer great advantages. In this study, we examine discrimination by foraging bees among flowers of nasturtium, Tropaeolum majus. Bee visitors included carpenter bees, Xylocopa violacea, which were primary nectar robbers; honeybees, Apis mellifera, which either acted as secondary nectar robbers or gathered pollen legitimately and bumblebees, Bombus hortorum, which were the only bees able to gather nectar legitimately. Many flowers were damaged by phytophagous insects. Nectar volume was markedly lower in flowers with damaged petals (which were also likely to be older) and in flowers that had nectar-robbing holes. We test whether bees exhibit selectivity with regards to the individual flowers, which they approach and enter, and whether this selectivity enhances foraging efficiency. The flowers approached (within 2 cm) by A. mellifera and B. hortorum were non-random when compared to the floral population; both species selectively approached un-blemished flowers. They both approached more yellow flowers than would be expected by chance, presumably a reflection of innate colour preferences, for nectar standing crop did not vary according to flower colour. Bees were also more likely to accept (land on) un-blemished flowers. A. mellifera gathering nectar exhibited selectivity with regards to the presence of robbing holes, being more likely to land on robbed flowers (they are not able to feed on un-robbed flowers). That they frequently approached un-robbed flowers suggests that they are not able to detect robbing holes at long-range, so that foraging efficiency may be limited by visual acuity. Nevertheless, by using a combination of long-range and short-range selectivity, nectar-gathering A. mellifera and B. hortorum greatly increased the average reward from the flowers on which they landed (by 68% and 48%, respectively) compared to the average standing crop in the flower population. Overall, our results demonstrate that bees use obvious floral cues (colour and petal blemishes) at long-range, but can switch to using more subtle cues (robbing holes) at close range. They also make many mistakes and some cues used do not correlate with floral rewards.     

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     

农药暴露的机制模型：蜜蜂毒理学的重要缺失

杀虫剂在最近的蜜蜂数量减少中所扮演的角色是有争议的,部分原因是实地研究常常无法检测到实验室研究所预测的效果。这种不一致性突出了蜜蜂毒理学研究领域的一个关键空白：对蜜蜂在它们的环境中杀虫剂暴露的模式和过程知之甚少。本文作者提出蜜蜂暴露杀虫剂的2个关键过程：1)工蜂采集花蜜的过程中收集农药;2)工蜂带回的农药在蜂巢中的再分配。工蜂收集农药的过程必须被理解为环境污染和蜜蜂觅食活动之间的时空交集。这意味着农药暴露是分配的,而不是离散的,觅食工蜂的一个子集可能会获得有害剂量的农药,而群体暴露将会显得安全。蜂箱中农药的分布是一个复杂的过程,主要是由群体成员之间食物转移的相互作用而产生,而这一过程中花粉和花蜜之间有重要的区别。因此应该优先将关于蜜蜂生物学的大量文献用于发展更严谨的蜂蜜农药暴露机制模型。与效应机制模型结合,暴露机制模型具有整合蜜蜂毒理学领域的潜力,以促进风险评估和基础研究。
精选自Sponsler, D. B. and Johnson, R. M. (2017), Mechanistic modeling of pesticide exposure: The missing keystone of honey bee toxicology. Environmental Toxicology and Chemistry, 36: 871–881. doi: 10.1002/etc.3661
详情请见http://onlinelibrary.wiley.com/doi/10.1002/etc.3661/full
     

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     

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 effects of colony-level selection on the social organization of honey bee (Apis mellifera L.) colonies: colony-level components of pollen hoarding

Two-way selection for quantities of stored pollen resulted in the production of high and low pollen hoarding strains of honey bees (Apis mellifera L.). Strains differed in areas of stored pollen after a single generation of selection and, by the third generation, the high strain colonies stored an average 6 times more pollen than low strain colonies. Colony-level organizational components that potentially affect pollen stores were identified that varied genetically within and between these strains. Changes occurred in several of these components, in addition to changes in the selected trait. High strain colonies had a significantly higher proportion of foragers returning with loads of pollen, however, high and low strain colonies had equal total numbers of foragers Colony rates of intake of pollen and nectar were not independent. Selection resulted in an increase in the number of pollen collectors and a decrease in the number of nectar collectors in high strain colonies, while the reciprocal relationship occurred in the low strain. High and low strain colonies also demonstrated different diurnal foraging patterns as measured by the changing proportions of returning pollen foragers. High strain colonies of generation 3 contained significantly less brood than did low strain colonies, a consequence of a constraint on colony growth resulting from a fixed nest volume and large quantities of stored pollen. These components represent selectable colony-level traits on which natural selection can act and shape the social organization of honey bee coloniesCommunicated by R.F.A. Moritz     

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.     

Honey bee foragers as sensory units of their colonies

Forager honey bees function not only as gatherers of food for their colonies, but also as sensory units shaped by natural selection to gather information regarding the location and profitability of forage sites. They transmit this information to colony members by means of waggle dances. To investigate the way bees transduce the stimulus of nectar-source profitability into the response of number of waggle runs, I performed experiments in which bees were stimulated with a sucrose solution feeder of known profitability and their dance responses were videorecorded. The results suggest that several attributes of this transduction process are adaptations to enhance a bee's effectiveness in reporting on a forage site. (1) Bees register the profitability of a nectar source not by sensing the energy gain per foraging trip or the rate of energy gain per trip, but evidently by sensing the energetic efficiency of their foraging. Perhaps this criterion of nectar-source profitability has been favored by natural selection because the foraging gains of honey bees are typically limited by energy expenditure rather than time availability. (2) There is a linear relationship between the stimulus of energetic efficiency of foraging and the response of number of waggle runs per dance. Such a simple stimulus-response function appears adequate because the range of suprathreshold stimuli (max/min ratio of about 10) is far smaller than the range of responses (max/min ratio of about 100). Although all bees show a linear stimulus-response function, there are large differences among individuals in both the response threshold and the slope of the stimulus-response function. This variation gives the colony a broader dynamic range in responding to food sources than if all bees had identical thresholds of dance response. (3) There is little or no adaptation in the dance response to a strong stimulus (tonic response). Thus each dancing bee reports on the current level of profitability of her forage site rather than the changes in its profitability. This seems appropriate since presumably it is the current profitability of a forage site, not the change in its profitability, which determines a site's attractiveness to other bees. (4) The level of forage-site quality that is the threshold for dancing is tuned by the bees in relation to forage availability. Bees operate with a lower dance threshold when forage is sparse than when it is abundant. Thus a colony utilizes input about a wide range of forage sites when food is scarce, but filters out input about low-reward sites when food is plentiful. (5) A dancing bee does not present her information in one spot within the hive but instead distributes it over much of the dance floor. Consequently, the dances for different forage sites are mixed together on the dance floor. This helps each bee following the dances to take a random sample of the dance information, which is appropriate for the foraging strategy of a honey bee colony since it is evidently designed to allocate foragers among forage sites in proportion to their profitability.     

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.     

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.     

An automated system for tracking and identifying individual nectar foragers at multiple feeders

Nectar-feeding animals have served as the subjects of many experimental studies and theoretical models of foraging. Their willingness to visit artificial feeders renders many species amenable to controlled experiments using mechanical “flowers” that replenish nectar automatically. However, the structural complexity of such feeders and the lack of a device for tracking the movements of multiple individuals have limited our ability to ask some specific questions related to natural foraging contexts, especially in competitive situations. To overcome such difficulties, we developed an experimental system for producing computer records of multiple foragers harvesting from simple artificial flowers with known rates of nectar secretion, using radio frequency identification (RFID) tags to identify individual animals. By using infrared detectors (light-emitting diodes and phototransistors) to activate the RFID readers momentarily when needed, our system prevents the RFID chips from heating up and disturbing the foraging behavior of focal animals. To demonstrate these advantages, we performed a preliminary experiment with a captive colony of bumble bees, Bombus impatiens. In the experiment, two bees were tagged with RFID chips (2.5 × 2.5 mm, manufactured by Hitachi-Maxell, Ltd., Tokyo, Japan) and allowed to forage on 16 artificial flowers arranged in a big flight cage. Using the resulting data set, we present details of how the bees increased their travel speed between flowers, while decreasing the average nectar crop per flower, as they gained experience. Our system provides a powerful tool to track the movement patterns, reward history, and long-term foraging performance of individual foragers at large spatial scales.     

Odour transfer in stingless bee marmelada (Frieseomelitta varia) demonstrates that entrance guards use an “undesirable–absent” recognition system

In group-level recognition, discriminators use sensory information to distinguish group members and non-members. For example, entrance guards in eusocial insect colonies discriminate nestmates from intruders by comparing their odour with a template of the colony odour. Despite being a species-rich group of eusocial bees closely related to the honey bees, stingless bee nestmate recognition is a relatively little-studied area. We studied Frieseomelitta varia, a common Brazilian species of stingless bee known as marmelada. By measuring the rejection rates of nestmate and non-nestmate worker bees by guards, we were able to show that guards became significantly less accepting (from 91 to 46%) of nestmates that had acquired odour cues from non-nestmate workers; however, guards did not become significantly more accepting (from 31 to 42%) of non-nestmates that had acquired equivalent amounts of odour cues from the guard’s nestmates. These data strongly suggest that guards use an “undesirable–absent” system in recognition, whereby incoming conspecific workers are only accepted if undesirable cues are absent, despite the presence of desirable cues. We suggest that an undesirable–absent system is adaptive because robbing by conspecifics may be an important selective factor in F. varia, which would lead to selection for a non-permissive acceptance strategy by guards.     

Social foraging in honey bees: how nectar foragers assess their colony's nutritional status

Summary A honey bee colony operates as a tightly integrated unit of behavioral action. One manifestation of this in the context of foraging is a colony's ability to adjust its selectivity among nectar sources in relation to its nutritional status. When a colony's food situation is good, it exploits only highly profitable patches of flowers, but when its situation is poor, a colony's foragers will exploit both highly profitable and less profitable flower patches. The nectar foragers in a colony acquire information about their colony's nutritional status by noting the difficulty of finding food storer bees to receive their nectar, rather than by evaluating directly the variables determining their colony's food situation: rate of nectar intake and amount of empty storage comb. (The food storer bees in a colony are the bees that collect nectar from returning foragers and store it in the honey combs. They are the age group (generally 12–18 day old bees) that is older than the nurse bees but younger than the foragers. Food storers make up approximately 20% of a colony members.) The mathematical theory for the behavior of queues indicates that the waiting time experienced by nectar foragers before unloading to food storers (queue length) is a reliable and sensitive indicator of a colony's nutritional status. Queue length is automatically determined by the ratio of two rates which are directly related to a colony's nutritional condition: the rate of arrival of loaded nectar foragers at the hive (arrival rate) and the rate of arrival of empty food storers at the nectar delivery area (service rate). These two rates are a function of the colony's nectar intake rate and its empty comb area, respectively. Although waiting time conveys crucial information about the colony's nutritional status, it has not been molded by natural selection to serve this purpose. Unlike signals, which are evolved specifically to convey information, this cue conveys information as an automatic by-product. Such cues may prove more important than signals in colony integration.     

Chemical signals in bumble bee foraging

Summary Foraging bumblebees (Bombus vosnesenskii) deposit a substance on rewarding flowers which assists in discrimination between rewarding and nonrewarding flowers in a controlled laboratory environment. Discrimination occurs while the bee is on a flower; workers probe rewarding flowers as well as empty ones that have rewarded in the recent past, but they do not probe flowers that have had no reward. Recognition is not the result of honey contamination left on the flower by the bee during feeding. The deposit is only slightly soluble in water or ethyl alcohol but is very soluble in pentane.     

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     

Directional change in a suite of foraging behaviors in tropical and temperate evolved honey bees (<Emphasis Type="Italic">Apis mellifera</Emphasis> L.)

The concept of a suite of foraging behaviors was introduced as a set of traits showing associative directional change as a characterization of adaptive evolution. I report how naturally selected differential sucrose response thresholds directionally affected a suite of honey bee foraging behaviors. Africanized and European honey bees were tested for their proboscis extension response thresholds to ascending sucrose concentrations, reared in common European colonies and, captured returning from their earliest observed foraging flight. Race constrained sucrose response threshold such that Africanized bees had significantly lower sucrose response thresholds. A Cox proportional hazards regression model of honey bee race and sucrose response threshold indicated that Africanized bees were 29% (P<0.01) more at risk to forage over the 30-day experimental period. Sucrose response threshold organized age of first foraging such that each unit decrease in sucrose response threshold increased risk to forage by 14.3% (P<0.0001). Africanized bees were more likely to return as pollen and water foragers than European foragers. Africanized foragers returned with nectar that was significantly less concentrated than European foragers. A comparative analysis of artificial and naturally selected populations with differential sucrose response thresholds and the common suite of directional change in foraging behaviors is discussed. A suite of foraging behaviors changed with a change in sucrose response threshold that appeared as a product of functional ecological adaptation.Communicated by R.F.A. Moritz     

A mark-recapture study of male<Emphasis Type="Italic"> Colletes cunicularius</Emphasis> bees: implications for pollination by sexual deception

An unusual pollination strategy is pollination by sexual deception in which orchids sexually attract male insects as pollinators. One gap in knowledge concerns the pattern and extent of pollinator movement among these sexually deceptive flowers and how this translates to pollen and gene flow. Our aim was to use mark and recapture techniques to investigate the behavior and movement of male Colletes cunicularius, an important bee pollinator of Ophrys. Our study site was located in northern Switzerland where a large population of the bees was nesting. Within two plots, (10×40 m), we marked bees with different colors and numbered tags. Seventeen percent of the 577 marked bees were recaptured over a period of 1 to a maximum of 11 days. However, the number of recaptures dropped dramatically after 3–5 days, suggesting an average lifetime of less than 10 days. Mark-recapture distances varied from 0 to 50 m, with a mean of 5 m. Our findings show that individual male bees patrol a specific and restricted region of the nesting area in search of mates. This mark-recapture study provides the first clues about the potential movement of pollen within populations of Ophrys orchids. We predict that orchid-pollen movements mediated by bees will be similar to the mark-recapture distances in this study. Parallel studies within orchid populations, including direct studies of pollen movement, are now required to better understand how pollinator mate-searching behavior translates to pollination success and pollen movement within sexually deceptive orchid populations.Communicated by R.F.A. Moritz     

Predation risk makes bees reject rewarding flowers and reduce foraging activity

In the absence of predators, pollinators can often maximize their foraging success by visiting the most rewarding flowers. However, if predators use those highly rewarding flowers to locate their prey, pollinators may benefit from changing their foraging preferences to accept less rewarding flowers. Previous studies have shown that some predators, such as crab spiders, indeed hunt preferentially on the most pollinator-attractive flowers. In order to determine whether predation risk can alter pollinator preferences, we conducted laboratory experiments on the foraging behavior of bumble bees (Bombus impatiens) when predation risk was associated with a particular reward level (measured here as sugar concentration). Bees foraged in arenas containing a choice of a high-reward and a low-reward artificial flower. On a bee’s first foraging trip, it was either lightly squeezed with forceps, to simulate a crab spider attack, or was allowed to forage safely. The foragers’ subsequent visits were recorded for between 1 and 4 h without any further simulated attacks. Compared to bees that foraged safely, bees that experienced a simulated attack on a low-reward artificial flower had reduced foraging activity. However, bees attacked on a high-reward artificial flower were more likely to visit low-reward artificial flowers on subsequent foraging trips. Forager body size, which is thought to affect vulnerability to capture by predators, did not have an effect on response to an attack. Predation risk can thus alter pollinator foraging behavior in ways that influence the number and reward level of flowers that are visited.     

Collective decision-making in honey bees: how colonies choose among nectar sources

Summary A honey bee colony can skillfully choose among nectar sources. It will selectively exploit the most profitable source in an array and will rapidly shift its foraging efforts following changes in the array. How does this colony-level ability emerge from the behavior of individual bees? The answer lies in understanding how bees modulate their colony's rates of recruitment and abandonment for nectar sources in accordance with the profitability of each source. A forager modulates its behavior in relation to nectar source profitability: as profitability increases, the tempo of foraging increases, the intensity of dancing increases, and the probability of abandoning the source decreases. How does a forager assess the profitability of its nectar source? Bees accomplish this without making comparisons among nectar sources. Neither do the foragers compare different nectar sources to determine the relative profitability of any one source, nor do the food storers compare different nectar loads and indicate the relative profitability of each load to the foragers. Instead, each forager knows only about its particular nectar source and independently calculates the absolute profitability of its source. Even though each of a colony's foragers operates with extremely limited information about the colony's food sources, together they will generate a coherent colonylevel response to different food sources in which better ones are heavily exploited and poorer ones are abandoned. This is shown by a computer simulation of nectar-source selection by a colony in which foragers behave as described above. Nectar-source selection by honey bee colonies is a process of natural selection among alternative nectar sources as foragers from more profitable sources survive (continue visiting their source) longer and reproduce (recruit other foragers) better than do foragers from less profitable sources. Hence this colonial decision-making is based on decentralized control. We suggest that honey bee colonies possess decentralized decision-making because it combines effectiveness with simplicity of communication and computation within a colony. Offprint requests to: T.D. Seeley