The role of a scent beacon in the communication of food location by the stingless bee, Melipona panamica

Melipona panamica foragers can deposit a scent beacon that influences the orientation of foragers near a food source. In misdirection experiments, newcomers (bees from the same colony as trained foragers) consistently preferred the feeder at which trained foragers had fed (training feeder) over an identical feeder at which bees had never fed (control feeder) even when the training feeder was placed at a site where experienced foragers had never foraged. Through similar misdirection experiments, the effective radius of the scent beacon was determined to be greater than 6 and less than 12 m. Foragers may deposit this beacon during a sequence of departure behaviors performed at the feeder. Prior to leaving the feeder with a load of sugar solution, bees tended to perform the following sequence of behaviors: (1) spinning, (2) grooming, (3) abdomen dragging, (4) excreting anal droplets, and (5) producing sounds, although not all behaviors were performed prior to each departure or at all sucrose concentrations (0.5–2.5 m). As sucrose concentration increased, the number of newcomers significantly increased, and the number of experienced foragers producing sounds and spinning on the feeder increased. The exact source of the scent beacon remains a mystery. However, three important sources have been excluded. When choosing between identical paired feeders, foragers were not attracted to the feeders with (1) anal droplets, (2) extracts of sucrose solution at which foragers had fed, or (3) mandibular gland extracts. They were indifferent to the first two preparations and exhibited only typical alarm behavior towards the mandibular gland (MG) extract: they oriented towards the feeder with MG extract but consistently landed on the feeder with no MG extract. Other authors have suggested that Melipona foragers deposit anal droplets to attract recruits, however the frequency of anal droplet production and the mass of anal droplets produced by M. panamica foragers are negatively correlated with sucrose concentration. Thus the scent beacon is evidently not deposited with anal droplets, infused into the feeder solution, or produced by mandibular glands. Received: 2 September 1997 / Accepted after revision: 30 January 1998     

The effect of ambient temperature on forager sound production and thoracic temperature in the stingless bee, <Emphasis Type="Italic">Melipona panamica</Emphasis>

Foragers of the stingless bees genus Melipona may produce intranidal sounds that are correlated with food location and quality. In this study, we provide the first detailed analysis of pulsed sounds produced by Melipona panamica foragers while feeding on a carbohydrate food source. We trained foragers to a 2.5-M sucrose feeder under normal, ambient temperature (23–33°C) and lower temperature (11–25°C) conditions. We recorded forager sounds under both conditions and tested the effect of temperature of the thorax, feeder plate, and air on sound temporal characteristics. Forager energetic expenditure and the number of pulses per visit were significantly higher in the cold condition than in the normal condition. Foragers spent a longer time at the feeder under the cold condition than during the normal condition. Interpulse durations were significantly shorter in the cold condition than in the normal condition and became progressively and significantly shorter at the end of each performance. Thus, pulse production increased before departure. Foragers increased their thoracic temperatures above ambient at all experimental air temperatures. Under chilled conditions, foragers had a significantly greater difference between thorax temperature and ambient air temperature than under normal conditions. Foragers must achieve a minimum flight muscle temperature before take-off, and thus forager sounds may be linked to muscle warm-up.     

Social foraging by honeybees: how colonies allocate foragers among patches of flowers

Summary To understand how a colony of honeybees keeps its forager force focussed on rich sources of food, and analysis was made of how the individual foragers within a colony decide to abandon or continue working (and perhaps even recruit to) patches of flowers. A nectar forager grades her behavior toward a patch in response to both the nectar intake rate of her colony and the quality of her patch. This results in the threshold in patch quality for acceptance of a patch being higher when the colonial intake rate of nectar is high than when it is low. Thus colonies can adjust their patch selectivity so that they focus on rich sources when forage is abundant, but spread their workers among a wider range of sources when forage is scarce. Foragers assess their colony's rate of nectar intake while in the nest, unloading nectar to receiver bees. The ease of unloading varies inversely with the colonial intake rate of nectar. Foragers assess patch quality while in the field, collecting nectar. By grading their behavior steeply in relation to such patch variables as distance from the nest and nectar sweetness, foragers give their colony high sensitivity to differences in profitability among patches. When a patch's quality declines, its foragers reduce their rate of visits to the patch. This diminishes the flow of nectar from the poor patch which in turn stimulates recruitment to rich patches. Thus a colony can swiftly redistribute its forager force following changes in the spatial distribution of rich food sources. The fundamental currency of nectar patch quality is not net rate of energy intake, (Gain-Cost)/Time, but may be net energy efficiency, (Gain-Cost)/Cost.     

Recruitment to food by the German yellowjacket, Vespula germanica

The hypothesis that Vespula germanica foragers can recruit nestmates to food resources was tested using a protocol that controlled for the biasing effects of social factors at the resource, including local enhancement and food-site marking substances. Foragers from an observation colony in the field were trained to visit a dish of scented corn syrup solution 15?m east of the nest. A second feeding station, 22?m northeast of the nest, offered incoming foragers a choice between food with the training scent and food with a control scent. Significantly more naive foragers arriving at that station chose the food with the training scent. We conclude that the German yellowjacket is able to recruit nestmates to carbohydrate food sources, and that recruits use food odor to locate the source of food being brought into the nest.     

A stingless bee (Melipona panamica) indicates food location without using a scent trail

The study of location specification in recruitment communication by bees has focused on two dimensions: direction and distance from the nest. Yet the third dimension, height above ground, may be significant in the tall and dense forest habitats of stingless bees. Foragers of the stingless bee Scaptotrigona postica recruit to a specific three-dimensional location by laying a scent trail. Stingless bees in the genus Melipona are thought to have a more sophisticated recruitment system that communicates distance through sounds inside the nest and direction through pointing zig-zag flights outside the nest. However, prior research on Melipona has not examined height communication or even established that foragers can recruit newcomers to a specific location. We used identical paired feeders to investigate recruitment to food in M panamica on Barro Colorado Island, Panama. We trained foragers from an observation hive to one feeder and monitored both feeders for the subsequent arrival of newcomers. We changed the relative positions of the feeders to test for correct direction, distance, and canopy-level communication. A 40-m canopy tower located inside the forest enabled us to examine canopy-level communication. We found that M. panamica foragers can recruit to a specific (1) direction, (2) distance, and (3) canopy level. To test the possibility that foragers accomplish this by means of a scent trail, we placed the colony on one shore of a small cove and trained bees over 116 m of open water to a feeder located on the opposite shore. We also placed a second feeder on this shore, equidistant from the colony but 20 m from the first feeder. Significantly more newcomers consistently arrived at the feeder visited by the foragers. Thus foragers evidently do not need a scent trail to communicate direction. Inside the nest, a forager produces pulsed sounds while visibly vibrating her wings after returning from a good food source. She is attended by other bees who cluster and hold their antennae around her, following her as she rapidly spins clockwise and counterclockwise. Locational information may be encoded in this behavior. However, foragers may also directly lead newcomers to the food source. Further experiments are planned to test for such piloting and other communication mechanisms.     

Propagation of olfactory information within the honeybee hive

Transfer of information about food source characteristics within insect societies is essential to colony-foraging success. The food odor communicated within honeybee hives has been shown to be important for food source exploitation. When successful foragers return to the nest and transfer the collected nectar to hive mates through mouth-to-mouth contacts (trophallaxis), potential recruits receiving these samples learn the food odor by associative learning. The food then becomes rapidly distributed among colony members, which is mainly a consequence of the numerous trophallaxes between hive-mates of all ages during food processing. We tested whether the distribution of food among hive mates causes a propagation of olfactory information within the hive. Using the proboscis extension response paradigm, we show that large proportions of bees of the age groups representing the main worker castes, 4 to 9-day-old bees (nurse-aged bees), 12 to 16-day-old bees (food processor-aged bees), and actual foragers (about 17+ day old bees) associatively learn the food odor in the course of processing food that has been collected by only a few foragers. Results further suggest that the information is shared more or less equally between bees of the three age groups. This shows that olfactory information about the flower species exploited by foragers is distributed within the entire colony and is acquired by bees of all age groups, which may influence many behaviors inside and outside the hive.     

The importance of experience in the interpretation of conspecific chemical signals

Foraging bumblebees scent mark flowers with hydrocarbon secretions. Several studies have found these scent marks act as a repellent to bee foragers. This was thought to minimize the risk of visiting recently depleted flowers. Some studies, however, have found a reverse, attractive effect of scent marks left on flowers. Do bees mark flowers with different scents, or could the same scent be interpreted differently depending on the bees’ previous experience with reward levels in flowers? We use a simple experimental design to investigate if the scent marks can become attractive when bees forage on artificial flowers that remain rewarding upon the bees’ return after having depleted them. We contrast this with bees trained in the more natural scenario where revisits to recently emptied flowers are unrewarding. The bees’ association between scent mark and reward value was tested with flowers scent marked from the same source. We find that the bees’ experience with the level of reward determines how the scent mark is interpreted: the same scent can act as both an attractant and a repellent. How experience and learning influence the interpretation of the meaning of chemical signals deposited by animals for communication has rarely been investigated.     

Decision making in ant foragers (<Emphasis Type="Italic">Lasius niger</Emphasis>) facing conflicting private and social information

Foragers of many ant species use pheromone trails to guide nestmates to food sources. During foraging, individual workers can also learn the route to a food source. Foragers of the mass-recruiting ant Lasius niger use both pheromone trails and memory to locate a food source. As a result, an experienced forager can have a conflict between social information (trail pheromones) and private information (route memory) at trail bifurcations. We tested decision making in L. niger foragers facing such an informational conflict in situations where both the strength of the pheromone trail and the number of previous visits to the food source varied. Foragers quickly learned the branch at a T bifurcation that leads to a food source, with 74.6% choosing correctly after one previous visit and 95.3% after three visits. Pheromone trails had a weaker effect on choice behaviour of naïve ants, with only 61.6% and 70.2% choosing the branch that had been marked by one or 20 foragers versus an unmarked branch. When there was a conflict between private and social information, memory overrides pheromone after just one previous visit to a food source. Most ants, 82–100%, chose the branch where they had collected food during previous foraging trips, with the proportion depending on the number of previous trips (1 v. 3) but not on the strength of the pheromone trail (1 v. 20). In addition, the presence of a pheromone trail at one branch in a bifurcation had no effect on the time it took an experienced ant to choose the correct branch (the branch without pheromone). These results suggest that private information (navigational memory) dominates over social information (chemical tail) in orientation decisions during foraging activities in experienced L. niger foragers.     

Manuscript in preparation for <Emphasis Type="Italic">Behavioral Ecology and Sociobiology</Emphasis> Bumble bee pollen foraging regulation: role of pollen quality,storage levels,and odor

The regulation of protein collection through pollen foraging plays an important role in pollination and in the life of bee colonies that adjust their foraging to natural variation in pollen protein quality and temporal availability. Bumble bees occupy a wide range of habitats from the Nearctic to the Tropics in which they play an important role as pollinators. However, little is known about how a bumble bee colony regulates pollen collection. We manipulated protein quality and colony pollen stores in lab-reared colonies of the native North American bumble bee, Bombus impatiens. We debut evidence that bumble bee colony foraging levels and pollen storage behavior are tuned to the protein quality (range tested: 17–30% protein by dry mass) of pollen collected by foragers and to the amount of stored pollen inside the colony. Pollen foraging levels (number of bees exiting the nest) significantly increased by 55%, and the frequency with which foragers stored pollen in pots significantly increased by 233% for pollen with higher compared to lower protein quality. The number of foragers exiting the nest significantly decreased (by 28%) when we added one pollen load equivalent each 5 min to already high intranidal pollen stores. In addition, pollen odor pumped into the nest is sufficient to increase the number of exiting foragers by 27%. Foragers directly inspected pollen pots at a constant rate over 24 h, presumably to assess pollen levels. Thus, pollen stores can act as an information center regulating colony-level foraging according to pollen protein quality and colony need. An erratum to this article can be found at     

Effect of food location and quality on recruitment sounds and success in two stingless bees,<Emphasis Type="Italic"> Melipona mandacaia</Emphasis> and<Emphasis Type="Italic"> Melipona bicolor</Emphasis>

It is unclear whether stingless bees in the genus Melipona (Hymenoptera, Apidae, Meliponini) can reliably encode the distance to a food source through recruitment sounds produced inside the nest, in part because the sound features correlated with distance also vary with food quality. We therefore trained marked foragers of two species, Melipona mandacaia and M. bicolor, to feeders at different distances and to different sucrose concentrations at the same distance. In both species, foragers successfully recruited to a rich 2.5-m food source and produced pulsed recruitment sounds in which pulse duration was significantly and positively correlated with distance to the rich food source. When returning from poorer food sources (0.6–1.5 m), foragers of both species decreased sound production, producing shorter sound pulses and longer sound interpulses than they did for 2.5 m food located at the same distance. Thus the temporal structure of M. mandacaia and M. bicolor recruitment sounds varies with distance and food quality. However, nestmates were not recruited by performances for poorer food sources (0.6–1.5 m), whose sucrose concentration was sufficiently low to affect recruitment sounds. Surprisingly, the interphase (the time between behavioral phases that communicate location) also increases with decreasing food quality in the closely related honeybees (Apis), suggesting a potential homology in the effect of food quality on the recruitment systems of Apis and Melipona. We explore the evolutionary implications of these similarities.Communicated by M. Giurfa     

Honeybee recruitment to scented food sources: correlations between in-hive social interactions and foraging decisions

Information exchange of environmental cues facilitates decision-making processes among members of insect societies. In honeybee foraging, it is unknown how the odor cues of a resource are relayed to inactive nest mates to enable resource exploitation at specific scented sources. It is presumed that bees need to follow the dance or to be involved in trophallaxis with a successful forager to obtain the discovered floral scent. With this in mind, we evaluated the influence of food scent relayed through in-hive interactions and the subsequent food choices. Results obtained from five colonies demonstrated that bees arriving at a feeding area preferred to land at a feeder carrying the odor currently exploited by the trained forager. The bees that landed at this feeder also showed more in-hive encounters with the trained forager than the individuals that landed at the alternative scented feeder. The most frequent interactions before landing at the correct feeder were body contacts with the active forager, a behavior that involves neither dance following nor trophallaxis. In addition, a reasonable proportion of successful newcomers showed no conspicuous interactions with the active forager. Results suggest that different sources of information can be integrated inside the hive to establish an odor-rewarded association useful to direct honeybees to a feeding site. For example, simple contacts with foragers or food exchanges with non-active foragers seem to be enough to choose a feeding site that carries the same scent collected by the focal forager.     

Exploration and exploitation of food sources by social insect colonies: a revision of the scout-recruit concept

Social insect colonies need to explore and exploit multiple food sources simultaneously and efficiently. At the individual level, this colony-level behaviour has been thought to be taken care of by two types of individual: scouts that independently search for food, and recruits that are directed by nest mates to a food source. However, recent analyses show that this strict division of labour between scouts and recruits is untenable. Therefore, a modified concept is presented here that comprises the possible behavioural states of an individual forager (novice forager, scout, recruit, employed forager, unemployed experienced forager, inspector and reactivated forager) and the transitions between them. The available empirical data are reviewed in the light of both the old and the new concept, and probabilities for the different transitions are derived for the case of the honey-bee. The modified concept distinguishes three types of foragers that may be involved in the exploration behaviour of the colony: novice bees that become scouts, unemployed experienced bees that scout, and lost recruits, i.e. bees that discover a food source other than the one to which they were directed to by their nest mates. An advantage of the modified concept is that it allows for a better comparison of studies investigating the different roles performed by social insect foragers during their individual foraging histories. Received: 29 December 1999 / Revised: 25 February 2000 / Accepted: 16 October 2000     

The use of waggle dance information by honey bees throughout their foraging careers

We studied the extent to which worker honey bees acquire information from waggle dances throughout their careers as foragers. Small groups of foragers were monitored from time of orientation flights to time of death and all in-hive behaviors relating to foraging were recorded. In the context of a novice forager finding her first food source, 60% of the bees relied, at least in part, on acquiring information from waggle dances (being recruited) rather than searching independently (scouting). In the context of an experienced forager whose foraging has been interrupted, 37% of the time the bees resumed foraging by following waggle dances (being reactivated) rather than examining the food source on their own (inspecting). And in the context of an experienced forager engaged in foraging, 17% of the time the bees initiated a foraging trip by following a waggle dance. Such dance following was observed much more often after an unsuccessful than after a successful foraging trip. Successful foragers often followed dances just briefly, perhaps to confirm that the kind of flowers they had been visiting were still yielding forage. Overall, waggle dance following for food discovery accounted for 12–25% of all interactions with dancers (9% by novice foragers and 3–16% by experienced foragers) whereas dance following for reactivation and confirmation accounted for the other 75–88% (26% for reactivation and 49–62% for confirmation). We conclude that foragers make extensive use of the waggle dance not only to start work at new, unfamiliar food sources but also to resume work at old, familiar food sources.     

Honeybees modify gustatory responsiveness after receiving nectar from foragers within the hive

Food quality is a relevant characteristic to be transferred within eusocial insect colonies because its evaluation improves the collective foraging efficiency. In honeybees, colony mates could directly acquire this resource characteristic during trophallactic encounters with nectar foragers. In the present study, we focused on the gustatory responsiveness of bees that have unloaded food from incoming foragers. The sugar sensitivity of receiver bees was assessed in the laboratory by using the proboscis extension response paradigm. After unloading, hive bees were captured either from a colony that foraged freely in the environmental surroundings or from a colony that foraged at an artificial feeder with a known sucrose solution. In the first situation, the sugar sensitivity of the hive bees negatively correlated with the sugar concentration of the nectar crops brought back by forager mates. Similarly, in the controlled situation, the highest sucrose concentration the receivers accepted during trophallaxis corresponded to the highest thresholds to sucrose. The results indicate that first-order receivers modify their sugar sensitivity according to the quality of the food previously transferred through trophallaxis by the incoming foragers. In addition, trophallaxis is a mechanism capable of transferring gustatory information in honeybees. Its implications at a social scale might involve changes in the social information as well as in nectar distribution within the colony.     

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     

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     

Potential mechanisms for the communication of height and distance by a stingless bee, Melipona panamica

This study investigates the recruitment communication mechanisms of a stingless bee, Melipona panamica, whose foragers can evidently communicate the three-dimensional location of a good food source. To determine if the bees communicate location information inside or outside the nest, we conducted removal experiments by training marked foragers to one of two identical feeders and then separating these experienced foragers from potential recruits as they left the nest. The feeders were positioned to test the communication of each dimension. The results show that recruits do not simply follow experienced foragers to the food source. Height and distance are communicated within the nest, while direction is communicated outside the nest. We then examined the pulsed sounds produced by recruiting foragers. While unloading food, recruiting foragers produced several short pulses and one or more very long pulses. On average, the longest unloading pulse per performance was 31–50% longer (P ≤ 0.018) for bees foraging on the forest floor than for bees foraging at the top of the forest canopy (40 m high). While dancing, recruiting foragers produced sound pulses whose duration was positively correlated with the distance to the food source (P < 0.001). Dancing recruiters also produced several short sound pulses followed by one or more long pulses. The longest dance pulse per performance was 291 ± 194 ms for a feeder 25 m from the nest and 1858 ± 923 ms for a feeder 360 m away from the nest. The mechanism of directional communication remains a mystery. However, the direction removal experiment demonstrates that newcomers cannot use forager-deposited scent marks for long-distance orientation (>100 m from the nest). Received: 25 September 1997 / Accepted after revision: 31 May 1998     

Reward rate and forager activation in honeybees: recruiting mechanisms and temporal distribution of arrivals

We analyzed the foraging and recruitment activity of single foragers ( Apis mellifera), exploiting low reward rates of sucrose solution. Single employed foragers (test bees) were allowed to collect 2.0 m sucrose solution delivered by a rate-feeder located at 160 m from the hive for 2 h. Flow rates varied between 1.4 and 5.5 µl/min. The individual behavior of the test bees was registered both at the hive and the food source, and the social output was calculated as the number of incoming bees arriving at the feeder per hour (henceforth: arrival rate). Incoming bees were captured once they landed at the feeder and assigned to one of three categories according to their foraging experience and hive interactions with the test bee: inspector, reactivated, or inexperienced bees. Both the waggle-runs performed per hour of foraging by test bees and the social output attained, increased with the reward rate. Also the number of hive-stays and the trophallactic-offering contacts performed by test bees were positively correlated with the arrival rate. For the highest reward rates, the duration of Nasonov-gland exposure at the feeding place was higher, and the arrival of most of the incoming bees occurred shortly after the test bee landed at the feeding platform. Thus, in addition to hive-interactions, landing of incoming bees at the food source is promoted by olfactory and/or visual information provided by the test bees. The proportions of inspector, reactivated, and inexperienced bees changed depending on the reward rate offered. Therefore, not only the occurrence and intensity of the recruitment-related behaviors performed by the test bees, but also the stimulation required by each category of incoming bees, determined the social output observed.