Repellent scent-marking of flowers by a guild of foraging bumblebees (Bombus spp.)

We have found that foraging bumblebees (Bombus hortorum, B. pascuorum, B. pratorum and B.␣terrestris) not only avoid flowers of Symphytum officinale that have recently been visited by conspecifics but also those that have been recently visited by heterospecifics. We propose that the decision whether to reject or accept a flower is influenced by a chemical odour that is left on the corolla by a forager, which temporarily repels subsequent foragers. Honeybees and carpenter bees have previously been shown to use similar repellent forage-marking scents. We found that flowers were repellent to other bumblebee foragers for approximately 20 min and also that after this time nectar levels in S. officinale flowers had largely replenished. Thus bumblebees could forage more efficiently by avoiding flowers with low rewards. Flowers to which extracts of tarsal components were applied were more often rejected by wild B. terrestris workers than flowers that had head extracts applied, which in turn were more often rejected than flowers that had body extracts applied. Extracts from four Bombus species were equally repellent to foragers. The sites of production of the repellent scent and its evolutionary origins are discussed. Received: 24 November 1997 / Accepted after revision: 8 March 1998     

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.     

Net energetic advantage drives honey bees (Apis mellifera L) to nectar larceny in Vaccinium ashei Reade

Carpenter bees (Xylocopa spp.) act as primary nectar thieves in rabbiteye blueberry (Vaccinium ashei Reade), piercing corollas laterally to imbibe nectar at basal nectaries. Honey bees (Apis mellifera L) learn to visit these perforations and thus become secondary nectar thieves. We tested the hypothesis that honey bees make this behavioral switch in response to an energetic advantage realized by nectar-robbing flower visits. Nectar volume and sugar quantity were higher in intact than perforated flowers, but bees (robbers) visiting perforated flowers were able to extract a higher percentage of available nectar and sugar so that absolute amount of sugar (mg) removed by one bee visit is the same for each flower type. However, because perforated flowers facilitate higher rates of bee flower visitation and the same or higher rates of nectar ingestion, they are rendered more profitable than intact flowers in temporal terms. Accordingly, net energy (J) gain per second flower handling time was higher for robbers on most days sampled. We conclude that the majority evidence indicates an energetic advantage for honey bees that engage in secondary nectar thievery in V. ashei.Communicated by R. Page     

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.     

Innate movement rules in foraging bees: flight distances are affected by recent rewards and are correlated with choice of flower type

The non-random movement patterns of foraging bees are believed to increase their search efficiency. These patterns may be innate, or they may be learned through the bees’ early foraging experience. To identify the innate components of foraging rules, we characterized the flight of naive bumblebees, foraging on a non-patchy “field” of randomly scattered artificial flowers with three color displays. The flowers were randomly mixed and all three flower types offered equal nectar volumes. Visited flowers were refilled with probability 0.5. Flight distances, flight durations and nectar probing durations were determined and related to the bees’ recent experiences. The naive bees exhibited area-restricted search behavior, i.e., flew shorter distances following visits to rewarding flowers than after visits to empty flowers. Additionally, flight distances during flower-type transitions were longer than flight distances between flowers of the same type. The two movement rules operated together: flight distances were longest for flights between flower types following non-rewarding visits, shortest for within-type flights following rewarding visits. An increase in flight displacement during flower-type shifts was also observed in a second experiment, in which all three types were always rewarding. In this experiment, flower-type shifts were also accompanied by an increase in flight duration. Possible relationships between flight distances, flight durations and flower-type choice are discussed. Received: 20 November 1995/Accepted after revision: 10 May 1996     

Effects of experience and weather on foraging rate and pollen versus nectar collection in the bumblebee, Bombus terrestris

This study examines factors that affect foraging rate of free-flying bumblebees, Bombus terrestris, when collecting nectar, and also what factors determine whether they collect pollen or nectar. We show that nectar foraging rate (mass gathered per unit time) is positively correlated with worker size, in accordance with previous studies. It has been suggested that the greater foraging rate of large bees is due to their higher thermoregulatory capacity in cool conditions, but our data suggest that this is not so. Workers differing in size were not differentially affected by the weather. Regardless of size, naïve bees were poor foragers, often using more resources than they gathered. Foraging rate was not maximised until at least 30 trips had been made from the nest. Foraging rates were positively correlated with humidity, perhaps because nectar secretion rates were higher or evaporation of nectar lower at high humidity. Temperature, wind speed and cloud cover did not significantly influence foraging rate, within the summertime range that occurred during the study. Weather greatly influenced whether bees collected pollen or nectar. Pollen was preferably collected when it was warm, windy, and particularly when humidity was low; and preferably during the middle of the day. We suggest that bees collect pollen in dry conditions, and avoid collecting pollen when there is dew or rain-water droplets on the vegetation, which would make grooming pollen into the corbiculae difficult. Availability of sufficient dry days for pollen collection may be an important factor determining the success of bumblebee colonies.Communicated by M. Giurfa     

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.     

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.     

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.     

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.     

Food alert in bumblebees (Bombus terrestris): possible mechanisms and evolutionary implications

The return of a successful bumblebee forager stimulates nestmates to leave the nest and search for food. Here we investigate the mechanisms by which this happens. Successful Bombus terrestris foragers perform irregular runs in their nest, often lasting for several minutes. Run duration is at its maximum when food has just been discovered. Running likely serves to distribute a pheromone, since the information flow between "runners" and "recruits" can be disrupted by eliminating air exchange, while leaving other potential means of communication intact. In addition, nectar stores in the nest may be monitored continuously. A sudden influx of nectar into the nest also causes measurable increases in forager activity. The implications of bumblebee recruitment behavior for the evolution of communication in bees are discussed.     

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 occurrence and context of tremble dancing in free-foraging honey bees (<Emphasis Type="Italic">Apis mellifera</Emphasis>)

Nectar foraging in honey bees is regulated by several communication signals that are performed mainly by foragers. One of these signals is the tremble dance, which is consistently performed by foragers from a rich food source which, upon return to the hive, experience a long delay before unloading their nectar to a nectar receiver. Although tremble dancing has been studied extensively using artificial nectar sources, its occurrence and context in a more natural setting remain unknown. Therefore, this study tests the sufficiency of the current explanations for tremble dancing by free-foraging honey bees. The main finding is that only about half of the observations of tremble dancing, referred to as delay-type tremble dancing, are a result of difficulty in finding a nectar receiver. In the remaining observations, tremble dancing was initiated immediately upon entering the hive, referred to as non-delay-type tremble dancing. Non-delay tremble dancing was associated with first foraging successes, both in a forager's career and in a single day. More than 75% of tremble dancing was associated with good foraging conditions, as indicated by the dancer continuing to forage after dancing. However, at least some of the other cases were associated with deteriorated foraging conditions, such as the end of the day, after which foraging was discontinued. No common context could be identified that explains all cases of tremble dancing or the subset of non-delay-type tremble dancing. This study shows that the current explanations for the cause of the tremble dance are insufficient to explain all tremble dancing in honey bees that forage at natural food sources.     

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.     

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.     

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.     

Analysis of bumblebee visitation sequences within single bouts: implication of the overstrike effect on short-term memory

Pollinators whose foraging habitats consist of several plant types (species or morph) may continue to choose the plant type last visited because information about the type of plant last visited dominates over all other memory contents, in particular of short-term memory. In this study, I extracted this overstrike effect on the plant choices of pollinators by analyzing patterns of visitation sequences within a single round-trip between the hive and foraging patch (bout). First, I simulated the visitation sequences within single bouts with a model to show how factors, including the bees plant-type preferences, the arrangement of plants and the effect of overstrike on short-term memory, affect visitation sequences. Here, bees are assumed to forage in a patch consisting of two plant types (H and L). The model predicts that only the effect of overstrike on short-term memory causes assorted visitation sequences according to plant type (within-bout flower constancy). That is, if the overstrike-effect on short-term memory is the primary determinant of plant choice, then bees will fly to a type-L plant after visiting a type-L plant even if they predominantly visit type-H plants and vice versa. Next, I investigated individual bumblebees visitation sequences at a patch of artificial inflorescences with a set-up similar to that assumed in the model. Two types of inflorescences were arranged on a Cartesian grid. Assorted visitation sequences according to inflorescence type were observed, depending on the distances among inflorescences. This result supports the hypotheses that bees fly to the same plant type as that last visited because short-term memory is displaced (overstruck) with information about the most recently visited plant type.Communicated by M. Giurfa     

Risk aversion in hand-reared bananaquits

Summary To study risk aversion in hand-reared bananaquits (Coereba flaveola) we placed individuals in a cage with a 1 m² floral board having a random array of 85 yellow and 85 red artificial flowers. Flowers of one color were filled with the same quantity of nectar (constant flowers), whereas flowers of the other color were filled with variable quantities of nectar (variable flowers). The constant and variable flowers had identical mean contents, only their variances differed. After three presentations, the constant flowers were made variable and vice versa to control for color preferences. Naive foragers tended to avoid variable flowers. The degree of risk aversion was influenced by previous experience, the relative variability of the variable flowers, and flower color. Variable flowers having similar coefficients of variation, but different reward variables (volume or concentration) resulted in similar levels of risk aversion. Within single foraging episodes the following was observed: sequences of constant flowers increased while sequences of variable flowers remained similar to random foraging; the probability of revisiting a constant flower was higher than revisiting a variable flower; the average amount of nectar consumed from constant and variable flowers was similar within the assessment periods (prior to favoring constant flowers); the proportion of visits falling below the mean expected reward during the assessment period or its inverse (the proportion visited with at least the equivalent of the mean) may be a cue used for risk aversion; risk aversion persisted through long foraging bouts despite changed nectar distributions suggesting that the bananaquits did not track resource distributions well within foraging bouts.     

Anther-mimicking floral guides exploit a conflict between innate preference and learning in bumblebees (<Emphasis Type="Italic">Bombus terrestris</Emphasis>)

Bee-pollinated plants are frequently dichogamous: e.g. each flower has a discernable male and female phase, with only the male phase offering a pollen reward. Pollen-collecting bees should therefore discriminate against female-phase flowers to maximise their rate of pollen harvest, but this behaviour would reduce plant fitness due to inferior pollination. Here, we test the hypothesis that flowers use pollen-mimicking floral guides to prevent flower-phase discrimination. Such floral guides resemble pollen in spectral reflection properties and are widespread among angiosperm flowers. In an array of artificial flowers, bumblebees learned less well to discriminate between flower variants simulating different flowering phases when both flower variants carried an additional pollen-yellow guide mark. This effect depended crucially on the pollen-yellow colour of the guide mark and on its spatial position within the artificial flower. We suggest that floral guides evolved to inhibit flower-phase learning in bees by exploiting the innate colour preferences of their pollinators.     

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.