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.     

Fifteen-spined stickleback (Spinachia spinachia) females prefer males with more secretional threads in their nests: an honest-condition display by males

In the fifteen-spined stickleback (Spinachia spinachia), the male alone builds a nest and provides care for the eggs until they hatch. The nest is made of filamentous algae held together with shiny secretional threads of a glycoprotein, here called tangspiggin. Tangspiggin is produced by transformed kidney cells. I investigated how tangspiggin production was related to food intake by giving males low or high food rations. Males in the high-food group produced significantly more tangspiggin than those in the low-food group. Since low food rations did not lead to a significant drop in resting metabolic rate (oxygen consumption), tangspiggin production appears to be one of the first energy-demanding processes to be dropped during food deprivation. Among males given equal food rations, females preferred to mate with those with elevated levels of tangspiggin in their nests. Tangspiggin threads may signal safety for the offspring by keeping the eggs within the nest and protecting them from egg predators. Moreover, the threads become less shiny with age, due to particle deposition, and older nests that may house older (more valuable) eggs are thereby well camouflaged. Tangspiggin provides an honest signal of male condition, acting as an extra-bodily ornament, signaling direct benefits to females or possibly also indirect benefits of "good genes" from a male who is a successful forager.     

Food-exchange by foragers in the hive – a means of communication among honey bees?

Dancing and trophallactic behaviour of forager honey bees, Apis mellifera ligustica >Spinola, that returned from an automatic feeder with a regulated flow rate of 50% weight-to-weight sucrose solution (range: 0.76–7.65 μl/min) were studied in an observation hive. Behavioural parameters of dancing, such as probability, duration and dance tempo, increased with the nectar flow rate, though with very different response curves among bees. For trophallaxis (i.e. mouth-to-mouth exchange of food), the frequency of giving-contacts and the transfer rate of the nectar increased with the nectar flow rate. After unloading, foragers often approached other nest mates and begged for food before returning to the food source. This behaviour was less frequent at higher nectar flow rates. These results show that the profitability of a food source in terms of nectar flow rate had a quantitative representation in the hive through quantitative changes in trophallactic and dancing behaviour. The role of trophallaxis as a communication channel during recruitment is discussed. Received: 14 January 1995/Accepted after revision: 14 August 1995     

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.     

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     

Forager specialization and the control of nest repair in Polybia occidentalis Olivier (Hymenoptera : Vespidae)

We measured patterns of individual forager specialization and colony-wide rates of material input during periods of response to experimental nest damage and during control periods in three colonies of the tropical social wasp Polybia occidentalis.

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.     

Dominance and polyethism in the eusocial wasp Mischocyttarus mastigophorus (Hymenoptera: Vespidae)

Dominance interactions affected patterns of non-reproductive division of labor (polyethism) in the eusocial wasp Mischocyttarus mastigophorus. Socially dominant individuals foraged for food (nectar and insect prey) at lower rates than subordinate individuals. In contrast, dominant wasps performed most of the foraging for the wood pulp used in nest construction. Social dominance also affected partitioning of materials collected by foragers when they returned to the nest. Wood pulp loads were never shared with nest mates, while food loads, especially insect prey, were often partitioned with other wasps. Dominant individuals on the nest were more likely to take food from arriving foragers than subordinate individuals. The role of dominance interactions in regulating polyethism has evolved in the eusocial paper wasps (Polistinae). Both specialization by foragers and task partitioning have increased from basal genera (independent-founding wasps, including Mischo-cyttarus spp.) to more derived genera (swarm-founding Epiponini). Dominance interactions do not regulate forager specialization or task partitioning in epiponines. I hypothesize that these changes in polyethism were enabled by the evolution of increased colony size in the Epiponini. Received: 8 December 1997 / Accepted after revision: 28 March 1998     

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     

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.     

Exploitation of carbohydrate food sources in <Emphasis Type="Italic">Polybia occidentalis</Emphasis>: social cues influence foraging decisions in swarm-founding wasps

An efficient exploitation of carbohydrate food sources would be beneficial for social wasp species that store nectar within their nest. In the swarm-founding polistine wasp Polybia occidentalis, we now demonstrate that the decisions of when and where to forage are influenced by information from conspecifics. Only when foragers had been trained to collect at artificial carbohydrate feeders did newcomers (food-source-naive individuals) continuously arrive at these feeders during 2 h of experiment. In control tests, in which no forager had been trained, not a single newcomer alighted at any of the offered carbohydrate food sources. This indicates that, during the foraging process, a nest-based input provided by successful foragers must have stimulated nestmates to search for food. Once activated, the newcomers’ choice on where to collect was strongly influenced by field-based social information. The mere visual presence of accumulated conspecifics (wasp dummies placed on one of the feeders) attracted newcomers to the food sources. Interestingly, however, visual enhancement was not the only decision-biasing factor at the feeding site. In an experimental series where searching wasps had to choose between the experimental feeder at which 3 foragers continuously collected and the control feeder with nine wasp dummies, only 40% of the wasps chose the visually enhanced feeder. This points to the existence of additional mechanisms of local enhancement. The possibility that, in social wasps, recruitment is involved in the exploitation of carbohydrate food sources is discussed.     

Nest defense and central place foraging: A model and experiment

Summary A graphical model presented here indicates that a nest-defending forager should stay closer to its nest, forage for shorter times per patch, and deliver smaller loads than predicated for delivery rate maximization. The effect is more pronounced farther from the nest, so that if nest defense is especially important, the predator should leave far patches sooner than near ones, and deliver smaller loads from farther away. Moreover, if the attack rate at the nest is increased, the defending forager should move closer and deliver smaller prey.Experimental attacks with stuffed specimens at Gila woodpecker (Melanerpes uropygialis) nests produced the predicted changes in the foraging behavior of males, but not of females.Mated pairs may work as a team to pursue simultaneously two conflicting goals—food delivery and nest protection—both of which affect the survivorship of the young. Sexual dimorphism in monogamous species may result in part from specialization in these roles.     

Colony nutritional status modulates worker responses to foraging recruitment pheromone in the bumblebee Bombus terrestris

Foraging activity in social insects should be regulated by colony nutritional status and food availability, such that both the emission of, and response to, recruitment signals depend on current conditions. Using fully automatic radio-frequency identification (RFID) technology to follow the foraging activity of tagged bumblebees (Bombus terrestris) during 16,000 foraging bouts, we tested whether the cue provided by stored food (the number of full honeypots) could modulate the response of workers to the recruitment pheromone signal. Artificial foraging pheromones were applied to colonies with varied levels of food reserves. The response to recruitment pheromones was stronger in colonies with low food, resulting in more workers becoming active and more foraging bouts being performed. In addition to previous reports showing that in colonies with low food successful foragers perform more excited runs during which they release recruitment pheromone and inactive workers are more prone to leave the nest following nectar influx, our results indicate that evolution has shaped a third pathway that modulates bumblebee foraging activity, thus preventing needless energy expenditure and exposure to risk when food stores are already high. This new feedback loop is intriguing since it involves context-dependent response to a signal. It highlights the integration of information from both forager-released pheromones (signal) and nutritional status (cue) that occurs within individual workers before making the decision to start foraging. Our results support the emerging view that responses to pheromones may be less hardwired than commonly acknowledged. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

The tremble dance of the honey bee: message and meanings

Summary The nectar foragers of a honey bee colony, upon return to the hive, sometimes perform a mysterious behavior called the tremble dance. In performing this dance, a forager shakes her body back and forth, at the same time rotating her body axis by about 50° every second or so, all the while walking slowly across the comb. During the course of a dance, which on average lasts 30 min, the bee travels about the broodnest portion of the hive. It is shown experimentally that a forager will reliably perform this dance if she visits a highly profitable nectar source but upon return to the hive experiences great difficulty finding a food-storer bee to take her nectar. This suggests that the message of the tremble dance is I have visited a rich nectar source worthy of greater exploitation, but already we have more nectar coming into the hive than we can handle. It is also shown experimentally that the performance of tremble dances is followed quickly by a rise in a colony's nectar processing capacity and (see Nieh, in press and Kirchner, submitted) by a drop in a colony's recruitment of additional bees to nectar sources. These findings suggest that the tremble dance has multiple meanings. For bees working inside the hive, its meaning is apparently I should switch to the task of processing nectar, while for bees working outside the hive (gathering nectar), its meaning is apparently I should refrain from recruiting additional foragers to my nectar source. Hence it appears that the tremble dance functions as a mechanism for keeping a colony's nectar processing rate matched with its nectar intake rate at times of greatly increased nectar influx. Evidently the tremble dance restores this match in part by stimulating a rise in the processing rate, and in part by inhibiting any further rise in the intake rate. Correspondence to: T. Seeley     

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.     

Does egg colour affect predation rate on open passerine nests?

The breeding success of many passerines is strongly reduced by egg predation. The adaptive significance of egg crypsis in open nesters is often taken for granted, but visually searching predators may first detect the nest or adult bird and not the eggs. Götmark predicted that selection should favour egg crypsis in the absence of conspicuous nests, whereas birds with conspicuous nests should have non-cryptic eggs. I compared the effect of egg colour treatment (white, blue, brown-spotted) on nest survival (1) among species characterized by different egg coloration, nest size and nest placement, and (2) between relatively well and poorly concealed nests within species. I used artificial nests (n=1,296) and eggs mimicking (except in egg colour) those of the yellowhammer (Emberiza citrinella), blackcap (Sylvia atricapilla) and song thrush (Turdus philomelos). Concurrently, I monitored survival of real nests (n=1,106). Nest survival differed among species, increased with nest concealment and throughout the breeding season, but was not significantly related to egg colour in any species. Nevertheless, the data for the yellowhammer suggest a trend in survival rates across the colour treatments. Brown eggs survived better than white eggs by 11% and 4% in 2 years, but this study had insufficient power to detect effects of this size. The results thus suggest that egg coloration in the song thrush and blackcap (shrub nesters) may be a neutral trait with regard to nest predation, whereas egg crypsis may be an anti-predation feature for the yellowhammer (ground/near-ground nester). The role of predation in the evolution of eggshell colour may vary not only between cavity and open nesters, but also across nest sites within the latter group.     

Trail and recruitment pheromones in Camponotus socius (Hymenoptera: Formicidae)

Summary. Worker ants of Camponotus socius employ multicomponent signals during group recruitment to food sources and nest emigrations. The chemical signals consist of trail orientation pheromones that originate from the hindgut. Two components that elicit trail orientation behavior were identified: (2S,4R,5S)-2,4-dimethyl-5-hexanolide and 2,3-dihydro-3,5-dihydroxy-6-methylpyran-4-one. Although both compounds release trail following behavior, in choice tests the former compound is preferred significantly. The major recruitment signal appears to be formic acid discharged from the poison gland. Compounds identified in the Dufour gland secretions do not seem to be involved in the recruitment process.     

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     

The role of internal and external information in foraging decisions of Melipona workers (Hymenoptera: Meliponinae)

Social insect foragers have to make foraging decisions based on information that may come from two different sources: information learned and memorised through their own experience (“internal” information) and information communicated by nest mates or directly obtained from their environment (“external” information). The role of these sources of information in decision-making by foragers was studied observationally and experimentally in stingless bees of the genus Melipona. Once a Melipona forager had started its food-collecting career, its decisions to initiate, continue or stop its daily collecting activity were mainly based upon previous experience (activity on previous days, the time at which foraging was initiated the day(s) before, and, during the day, the success of the last foraging flights) and mediated through direct interaction with the food source (load size harvested and time to collect a load). External information provided by returning foragers advanced the start of foraging of experienced bees. Most inexperienced bees initiated their foraging day after successful foragers had returned to the hive. The start of foraging by other inexperienced bees was stimulated by high waste-removal activity of nest mates. By experimentally controlling the entries of foragers (hence external information input) it was shown that very low levels of external information input had large effect on the departure of experienced foragers. After the return of a single successful forager, or five foragers together, the rate of forager exits increased dramatically for 15 min. Only the first and second entry events had large effect; later entries influenced forager exit patterns only slightly. The results show that Melipona foragers make decisions based upon their own experience and that communication stimulates these foragers if it concerns the previously visited source. We discuss the organisation of individual foraging in Melipona and Apis mellifera and are led to the conclusion that these species behave very similarly and that an information-integration model (derived from Fig. 1) could be a starting point for future research on social insect foraging. Received: 16 April 1997 / Accepted after revision: 30 August 1997     

Balancing between mutualism and exploitation: the symbiotic interaction between Lasius ants and aphids

Nests of Lasius niger (L.) ants were given varied food regimens to test whether their behaviour towards an aphid partner, Aphis fabae (Scop.), changed with alternative food supplies. Honeydew collection and predation on aphids were measured by video monitoring the movement of ants between their nest and an aphid aggregation. Data collected from the aphid aggregations enabled comparisons between remaining aphid biomass and between the tending intensities of the ants. I tested how ant behaviour was influenced by their access to alternative prey and sugar. The results showed that ants accepted a honey solution as a substitute for the honeydew produced by aphids. Ants not only attended their aphid partners, but also preyed on them. The average predation rate increased eightfold when ants were offered the alternative of sugar, whereas alternative prey had no significant effect. In contrast, ant-tending intensity decreased with alternative sugar whereas alternative prey elicited no effect.