Partial nectar loads as a cause of multiple nectar transfer in the honey bee (Apis mellifera): a simulation model

Honey bee foragers transfer their nectar loads to receiver bees within the nest. Surprisingly, they often transfer to more than one receiver (published values range from 1.9 to 2.7). Several adaptive hypotheses have been proposed to explain why multiple transfer occurs. One hypothesis, information improvement, states that multiple transfer arises as an adaptive forager-driven process. Foragers use the delay in finding a receiver to assess the relative work capacities of foragers and receivers, performing recruitment dances when appropriate. Multiple transferring improves their delay information. We used a stochastic simulation model to investigate the non-adaptive partial loads hypothesis. We determined the extent to which partial crop loads and receiver filling and emptying rules (i.e. how much nectar to accept before leaving the transfer area) can cause multiple transfer. As many as 1.9 nectar transfers per returning forager were generated within biologically realistic parameter space. We suggest that much multiple transfer arises as a non-adaptive consequence of partitioning nectar foraging between foragers and receivers, but that this will also result in foragers having better information about the relative work capacities of foragers and receivers as a useful consequence. We suggest that the number of transfers caused by partial loads could also be increased by an adaptive forager-driven effort to improve their information concerning the balance of foragers and receivers and we outline a framework wherein the information improvement hypothesis can be directly tested.     

Task Partitioning in Insect Societies. I. Effect of Colony Size on Queueing Delay and Colony Ergonomic Efficiency

The collection and handling of colony resources such as food, water, and nest construction material is often divided into subtasks in which the material is passed from one worker to another. This is known as task partitioning. When material is transferred directly from one individual to another, queueing delays frequently occur because individuals must sometimes wait for a transfer partner. A stochastic simulation model was written to study the effect of colony size on these delays. Queueing delay decreases roughly exponentially with colony size because stochastic fluctuations in the arrival of individuals are lower in larger colonies. These results support empirical studies of Polybia occidentalis and other theoretical studies of honeybees. The effect of the relative number of individuals in the two subtask groups was also studied. There is a unique optimal ratio of the number of workers associated with each of the subtasks that simultaneously minimizes mean queueing delay and maximizes colony nectar-processing rate. Deviations from this optimal ratio, for example, as a result of forager mortality or changes in nectar productivity that affect foraging trip duration, increase mean queueing delays greatly, especially in smaller colonies.     

The hidden cost of information in collective foraging

Many animals nest or roost colonially. At the start of a potential foraging period, they may set out independently or await information from returning foragers. When should such individuals act independently and when should they wait for information? In a social insect colony, for example, information transfer may greatly increase a recruit's probability of finding food, and it is commonly assumed that this will always increase the colony's net energy gain. We test this assumption with a mathematical model. Energy gain by a colony is a function both of the probability of finding food sources and of the duration of their availability. A key factor is the ratio of pro-active foragers to re-active foragers. When leaving the nest, pro-active foragers search for food independently, whereas re-active foragers rely on information from successful foragers to find food. Under certain conditions, the optimum strategy is totally independent (pro-active) foraging because potentially valuable information that re-active foragers may gain from successful foragers is not worth waiting for. This counter-intuitive outcome is remarkably robust over a wide range of parameters. It occurs because food sources are only available for a limited period. Our study emphasizes the importance of time constraints and the analysis of dynamics, not just steady states, to understand social insect foraging.     

Task-partitioned nectar transfer in stingless bees: work organisation in a phylogenetic context

Abstract 1. The eusocial corbiculate bee tribes comprise the Apini (honey bees), Bombini (bumble bees), and Meliponini (stingless bees). Honey bee foragers ( Apis ) transfer nectar to receiver bees within the nest. This is an example of task partitioning, in which a task is split into sub-tasks connected by material transfer. Nectar transfer does not occur in Bombini. Although it is reported in some species of Meliponini, it has not been subject to detailed study.
2. Nectar transfer was investigated in five genera of Meliponini from Yucatan, Mexico ( Melipona , Trigona , Scaptotrigona , Nannotrigona , and Plebeia ). Nectar transfer occurred in all species and for > 99% of foragers. Multiple transfer, in which a forager unloads nectar to more than one receiver, occurred but at a lower level than in Apis . In M. beecheii , multiple transfer was associated strongly with putative recruitment dances.
3. The data provide some support for the hypothesis that task partitioning is favoured by large colony size, in that the Meliponini never have small colonies because colonies are swarm founded. This ensures that colonies are always large enough to prevent delays in finding a transfer partner imposing high costs. Further tests of this hypothesis are suggested.
4. Viewed in a phylogenetic context, the most parsimonious interpretation is that nectar transfer evolved once in the clade (Apini + Meliponini).     

Nectar distribution and its relation to food quality in honeybee (<Emphasis Type="Italic">Apis mellifera</Emphasis>) colonies

In honeybees (Apis mellifera), the process of nectar collection is considered a straightforward example of task partitioning with two subtasks or two intersecting cycles of activity: (1) foraging and (2) storing of nectar, linked via its transfer between foragers and food processors. Many observations suggest, however, that nectar collection and processing in honeybees is a complex process, involving workers of other sub-castes and depending on variables such as resource profitability or the amount of stored honey. It has been observed that food processor bees often distribute food to other hive bees after receiving it from incoming foragers, instead of storing it immediately in honey cells. While there is little information about the sub-caste affiliation and the behaviour of these second-order receivers, this stage may be important for the rapid distribution of nutrients and related information. To investigate the identity of these second-order receivers, we quantified behaviours following nectar transfer and compared these behaviours with the behaviour of average worker hive-bees. Furthermore, we tested whether food quality (sugar concentration) affects the behaviour of the second-order receivers. Of all identified second-order receivers, 59.3% performed nurse duties, 18.5% performed food-processor duties and 22.2% performed forager duties. After food intake, these bees were more active, had more trophallaxes (especially offering contacts) compared to average workers and they were found mainly in the brood area, independent of food quality. Our results show that the liquid food can be distributed rapidly among many bees of the three main worker sub-castes, without being stored in honey cells first. Furthermore, the results suggest that the rapid distribution of food partly depends on the high activity of second-order receivers. Received 31 August 2006; revised 8 December 2006; accepted 11 December 2006.     

How long will honey bees (<Emphasis Type="Italic">Apis mellifera</Emphasis> L.) be stimulated by scent to revisit past-profitable forage sites?

Honey bees utilise floral food sources that vary temporally in their relative and absolute quality. Via a sophisticated colony organisation, a honey bee colony allocates its foragers such that the colony focuses on the most profitable forage sites while keeping track of changes within its foraging environment. One important mechanism of the allocation of foragers is the ability of experienced foragers to revisit past-profitable forage sites after a period of temporary dearth caused by, for example, inclement weather. The scent of past-profitable forage within the colony brought back by other foragers is sufficient to reactivate these experienced foragers. Here I determine for how long bees react to the scent of a past-profitable forage site. I show that the ability of foragers to revisit the location of a past-profitable food source diminishes rapidly over a period of 10 days, until no forager reacts to the cue (scent). I discuss the implications of these findings with respect to the colony’s ability to react rapidly to changing foraging conditions.     

Learning and time‐dependent cue choice in the desert ant,Melophorus bagoti

Foraging ants are known to use multiple sources of information to return to the nest. These cue sets are employed by independent navigational systems including path integration in the case of celestial cues and vision‐based learning in the case of terrestrial landmarks and the panorama. When cue sets are presented in conflict, the Australian desert ant species, Melophorus bagoti, will choose a compromise heading between the directions dictated by the cues or, when navigating on well‐known routes, foragers choose the direction indicated by the terrestrial cues of the panorama against the dictates of celestial cues. Here, we explore the roles of learning terrestrial cues and delays since cue exposure in these navigational decisions by testing restricted foragers with differing levels of terrestrial cue experience with the maximum (180°) cue conflict. Restricted foragers appear unable to extrapolate landmark information from the nest to a displacement site 8 m away. Given only one homeward experience, foragers can successfully orient using terrestrial cues, but this experience is not sufficient to override a conflicting vector. Terrestrial cue strength increases with multiple experiences and eventually overrides the celestial cues. This appears to be a dynamic choice as foragers discount the reliability of the terrestrial cues over time, reverting back to preferring the celestial vector when the forager has an immediate vector, but the forager's last exposure to the terrestrial cues was 24 hr in the past. Foragers may be employing navigational decision making that can be predicted by the temporal weighting rule.     

Crop scents affect the occurrence of trophallaxis among forager honeybees

Previous evidence indicates that the recognition of the nectar delivered by forager honeybees within the colony may have been a primitive method of communication on food resources. Thus, the association between scent and reward that nectar foragers establish while they collect on a given flower species should be retrieved during trophallaxis, i.e., the transfer of liquid food by mouth, and, accordingly, foraging experience could affect the occurrence of these interactions inside the nest. We used experimental arenas to analyze how crop scents carried by donor bees affect trophallaxis among foragers, i.e., donors and receivers, which differ in their foraging experience. Results showed that whenever the foragers had collected unscented sugar solution from a feeder the presence of scents in the solution carried by donors did not affect the occurrence of trophallaxis nor its dynamics. In contrast, whenever the foragers had previous olfactory information, new scents present in the crop of the donors negatively affected the occurrence, but not the dynamics of trophallaxis. Thus, the association learned at the food source seems to be retrieved during trophallaxis, and it is possible that known scents present in the mouthparts of nest-mates may operate as a triggering stimulus to elicit trophallactic behavior within the hive.     

Organization and Regulation of Nest Construction Behavior in Metapolybia Wasps

Field observations and experiments revealed that construction behavior of Metapolybia wasps is based on parallel processing and distributed decision making. Sixteen behaviors were used to separate five behavioral groupings: specialized water forager, flexible pulpforager, active builder, active generalist, and idle. The idle category proved to be the source and the sink of the other task groups, although specialist foragers tend to retain their duties or take over other active roles. Nest construction is partitioned into three tasks. Pulp foragers transfer wood-pulp to the nest where other wasps (builders) distribute and process it further. The builders incorporate this material into the nest structure on the basis of individual decisions. Water foragers provide the extra water necessary for both building and pulp collecting. Material exchange takes place on the nest between pairs or in small groups. The duration and frequency of different behaviors, the number of wasps belonging to different behavioral groups, and the different scale of specialization in different groups suggest that the colony-level performance and speed are governed by the activity of the pulp foragers, who receive information about both the water saturation level of the colony and the activity of the builders through local interactions. Several predictions of this hypothesis were supported by disturbing the normal construction behavior through removing or decreasing the number of individuals belonging to different behavioral groups or supplying additional building material.     

Head-on encounter rates and walking speed of foragers in leaf-cutting ant traffic

Summary. Trail traffic of the leaf-cutting ant Atta cephalotes involves intermingled flows of outbound and returning foragers. Head-on encounters between workers from the opposite flows are a common occurrence in this traffic. Each encounter momentarily delays the two ants involved, and these small delays might pose a significant cost to the colony's foraging performance when summed over thousands of workers along many metres of trail. We videotaped outbound and returning foragers over a 1 m course, and measured the encounter rates they experienced and their velocity. Our analysis indicates that locomotion speed is diminished by increasing encounter rate, but that the effect is small relative to the effects of ant body size and load mass. Head-on encounters allow exchange of information and leaf fragments between workers, and we consider how the benefits of such encounters may make this form of traffic organization superior to segregated outbound and returning lanes, despite the measurable c ost of encounters in mixed traffic.     

Trophallaxis in forager honeybees (<Emphasis Type="Italic">Apis mellifera</Emphasis>): resource uncertainty enhances begging contacts?

Trophallaxis among adult worker honeybees is the transfer of liquid food by mouth from one individual to another. Within the colony, nectar foragers perform offering contacts (as food-donors) to transfer the contents of their crops to recipient nest-mates and, in addition, they also perform begging contacts (as food-receivers). The biological relevance of these last interactions remains unknown. Previous evidence suggests that begging may be involved in the exchange of information on food resources that occurs naturally between employed foragers and nest-mates. This work was aimed to reveal possible connections between the information obtained while foraging and the begging behavior displayed inside the nest. Experiments were intended to (1) analyze whether chemosensory information obtained while foraging, i.e., odors and sucrose concentrations, affects begging behavior, and (2) determine whether resource uncertainty enhances begging contacts. Results showed that: (1) most begging contacts lasted less than 1 s, a duration which only allows receiving food samples from nest-mates; (2) the diversity of odors and sucrose concentrations at the feeding place enhances the occurrence of begging contacts; and (3) an increased resource uncertainty enhances the forager begging behavior. In addition, results suggest that foragers may direct their begging contacts frequently to other employed nectar foragers.     

An exploration of the relationship between recruitment communication and foraging in stingless bees

Social information is widely used in the animal kingdom and can be highly adaptive. In social insects, foragers can use social information to find food, avoid danger, or choose a new nest site. Copying others allows individuals to obtain information without having to sample the environment. When foragers communicate information they will often only advertise high-quality food sources, thereby filtering out less adaptive information. Stingless bees, a large pantropical group of highly eusocial bees, face intense inter- and intra-specific competition for limited resources, yet display disparate foraging strategies. Within the same environment there are species that communicate the location of food resources to nest-mates and species that do not. Our current understanding of why some species communicate foraging sites while others do not is limited. Studying freely foraging colonies of several co-existing stingless bee species in Brazil, we investigated if recruitment to specific food locations is linked to 1) the sugar content of forage, 2) the duration of foraging trips, and 3) the variation in activity of a colony from 1 day to another and the variation in activity in a species over a day. We found that, contrary to our expectations, species with recruitment communication did not return with higher quality forage than species that do not recruit nestmates. Furthermore, foragers from recruiting species did not have shorter foraging trip durations than those from weakly recruiting species. Given the intense inter- and intraspecific competition for resources in these environments, it may be that recruiting species favor food resources that can be monopolized by the colony rather than food sources that offer high-quality rewards.     

Behaviour of worker subcastes in the fire ant, Solenopsis invicta, in response to proteinaceous food

ABSTRACT. The effects of division of labour on response behaviour to food in the red imported fire ant, Solenopsis invicta Buren, were examined to determine if caste members differ in amount of food taken, in rate of food transfer, or in internal distribution of food; and to see if food availability, time, or temporal subcaste pairing affect feeding behaviour. To measure differences in behaviour we fed radioiodinated albumin mixed with egg yolk to colonies containing larvae, queens, and (a) foragers and nurses, or (b) foragers and reserves, or (c) nurses and reserves. Samples were taken over a 72-h period and radioactivity in the head, thorax and abdomen of each worker was determined. There were significant differences between nurses, foragers and reserves in quantity of food consumed, rate of transfer, and internal distribution of radioactivity. These differences were related to their respective roles of foraging, food storage and transfer, and brood tending. The quantity of food taken per subcaste was dependent on the total amount of food in the colony, with transfer rates differing between subcastes as the quantity of food in the colony increased. The rate at which protein was transferred between subcastes was slower in the reserves than that in either foragers or nurses. Therefore, reserves may serve as a temporary store of protein for the colony.     

Dynamic matching of forager size to resources in the continuously polymorphic leaf-cutter ant, Atta colombica (Hymenoptera, Formicidae)

Abstract.  1. Ergonomic optimisation theory proposes that by increasing variation in worker morphology, social insect colonies may increase their dietary breadth; however, little is known about how this relationship operates at the colony level. This study examines the colony-level pattern of forager size allocation to resource sites in a natural setting.
2. Using a biologically relevant measure of toughness, it is shown that leaf-cutter ant colonies exploit a variety of plant resources that vary significantly in toughness at any given time.
3. Forager size is shown to be matched to the toughness of plant material, with larger ants harvesting tougher material.
4. Furthermore, outbound foragers travelling to a harvest site are matched in size to the toughness of plant material contained within the site and are not a random selection of available foragers. The match between forager size and plant toughness may reduce the number of wasted trips and ill-matched foragers.
5. The observed colony-level pattern of forager allocation could be the result of learning by individual foragers, or the result of information shared at the colony level.     

Perception of the pollen need by foragers in a honeybee colony

Honeybees, Apis mellifera, adjust their pollen foraging activity according to the need for pollen within the colony, determined by the amount of stored pollen and young brood present in the hive. To clarify how pollen foragers detect the supply of pollen, we followed individual honeybees while they were returning with pollen. Pollen foragers deposited their loads on the frame where most of the unsealed brood was, independent of the position of this frame within the hive. They also inspected more cells on that frame and spent most of their time there, indicating that pollen foragers may individually evaluate the pollen requirements of the colony. In 18 normal-sized colonies we also tested whether olfactory cues provided by a frame of hungry young brood or an additional pollen frame covered by cages affect foraging activity. These experiments showed that olfactory stimulation within the colony is insufficient to increase or decrease the foraging effort, but suggest that foragers must have direct contact with the brood and pollen area to regulate their foraging activity according to the conditions in the colony. The different mechanisms by which foragers may gather the information about pollen supply are discussed. Copyright 2000 The Association for the Study of Animal Behaviour.     

Recruitment-dance signals draw larger audiences when honey bee colonies have multiple patrilines

Honey bee queens (Apis mellifera) who mate with multiple males produce colonies that are filled with numerous genetically distinct patrilines of workers. A genetically diverse colony benefits from an enhanced foraging effort, fuelled in part by an increase in the number of recruitment signals that are produced by foragers. However, the influence of patriline diversity on the attention paid to these signals by audiences of potentially receptive workers remains unexplored. To determine whether recruitment dances performed by foragers in multiple-patriline colonies attract a greater number of dance followers than dances in colonies that lack patriline diversity, we trained workers from multiple- and single-patriline colonies to forage in a greenhouse and monitored their dance-following activity back in the hives. On average, more workers followed a dance if it was performed in a multiple-patriline colony rather than a single-patriline colony (33% increase), and for a greater number of dance circuits per follower. Furthermore, dance-following workers in multiple-patriline colonies were more likely to exit their hive after following a dance, although this did not translate to a difference in colony-level exit rates between treatment types. Recruiting nest mates to profitable food sources through dance communication is critical to a colony’s foraging success and long-term fitness; polyandrous queens produce colonies that benefit not only from increased recruitment signalling, but also from the generation of larger and more attentive audiences of signal receivers. This study highlights the importance of integrating responses of both signal senders and receivers to understand more fully the success of animal-communication systems.     

Regulation of worker activity in a primitively eusocial wasp, Ropalidia marginata

Ropalidia marginala, a tropical, primitively eusocial, polistinewasp, is unusual in that the queen (the sole egg-layer) is neitherthe most behaviorally dominant nor the most active individualin the colony. The queen by herself rarely ever initiates interactionstoward her nest mates or unloads returning foragers. There arealways a few workers in the colony who are more dominant andactive than the queen. Absence of the queen from her colonydoes not affect colony maintenance activities such as foragingor brood care, but it always results in one individual becomingvery aggressive and dominant. The dominant worker becomes thenext queen if the original queen does not return. The queendoes not appear to play any significant role in colony activityregulation. Instead, colony activities appear to be regulatedby several mechanisms including dominance behavior toward foragers,feeding of larvae, and the unloading of returning foragers,all mediated by workers themselves. Regulation of colony maintenanceappears to be based on direct evaluation of the needs of thecolony by the workers themselves. The queen however has perfectreproductive control over all workers; workers never lay eggsin the presence of the queen. It appears therefore that themechanisms involved in regulation of worker activity and workerreproduction are separate in R marginata. These findings contrastwith other primitively eusocial species where the queen actsas a "central pacemaker" and controls both worker activity andworker reproduction.     

Bumble bees (Bombus terrestris) store both food and information in honeypots

Social insect foragers often transmit information about foodsources to nest mates. In bumble bees (Bombus terrestris), forexample, successful foragers use excited motor displays anda pheromone as communication signals. In addition, bees couldmake use of an indirect pathway of information flow, via thehoney stores. We show here that, indeed, bees in the nest continuouslymonitor honeypots and sample their contents, thus obtaininginformation on supply and demand of nectar. When there is aninflux of nectar into the nest, the colony deploys more workersfor foraging. The number of new foragers depends on sugar concentration.Foragers returning with high-quality sugar solution displaymore "excited runs" on the nest structure. The recruits' response,however, does not depend on modulated behavior by foragers:more workers start to forage with high quality of incoming nectar,even when this nectar is brought by a pipette. Moreover, weshow that the readiness of bees to respond to recruitment signalsor incoming nectar also depends on colony demand. When colonynectar stores are full, the response of bees to equal amountsof nectar influx is smaller than when stores are empty. Whencolony nectar stores are depleted, foragers spend more timerunning excitedly and less time probing pots in the nest andrun with higher average speed, possibly to disperse the alertingpheromone more efficiently. However, more bees respond to nectarinflux to empty stores, whether or not this is accompanied byforager signals. Thus, honeypots serve to store informationas well as food.     

Eavesdropping foragers use level of collective commotion as public information to target high quality patches

Public information offers a valuable means for social foragers to determine the relative quality of foraging patches. Despite much evidence that foragers use public information based on others’ feeding behavior, no experiments have examined whether foragers might use public information based on others’ competitive behavior, particularly the collective commotion that can be generated by aggregations. Such commotion could potentially provide a rich source of public information: as foragers compete in a patch with an especially high value resource, their heightened competition intensity could enable eavesdropping foragers to target this superior patch, based simply on its higher level of collective commotion. To test the hypothesis that the level of collective commotion is used as public information by eavesdropping foragers I conducted field experiments on terrestrial hermit crabs Coenobita compressus. These animals engage in collective competitive interactions in foraging patches for food and shells, generating variable levels of commotion across different quality patches. By experimentally manipulating the level of collective commotion in sham aggregations in the wild I show that a higher level of commotion is exploited by eavesdropping foragers to differentially target more valuable patches. Broadly, these results highlight an underappreciated significance of competitive by‐products and higher‐ order collective pheno mena as forms of public information for foragers.     

Seasonal foraging characteristics during mid-day of successful underground colonies of Vespula vulgaris (Hymenoptera, Vespidae) in England

Summary: The hourly transit rates and the number of forager types during the middle of the day are presented for successful colonies of V. vulgaris. Outgoing foragers are divided into earth carriers and non-earth outgoers. Incoming foragers are divided into pulp, flesh and fluid carriers, and empty incomers. Fluid carriers also are divided into full and partial fluid carriers. The transit rates of different colonies are expressed as a percentage of their highest transit rates so that data from different colonies can be considered together. The percentage values of each type of outgoing and incoming forager are calculated from the daily counts so that again, data from different colonies can be considered together. The total hourly number of foragers and forager types during the middle of the day is used to generate a model for a hypothetical larger and smaller colony, during the whole of the colony's existence. During a colony's existence, 27.5 % of the outgoers are earth carriers, and of the incomers, 12.2 % are pulp carriers, 12.0 % flesh carriers, 72.2 % fluid carriers, and 3.7 % empty incomers. The relative lack of earth carriers during the large-cell colony phase can be related to the use of the nocturnal resting space in which some of the large-cell combs are built. This space, at the bottom of the nest, was excavated and used by the workers during the small-cell colony phase. Empty incomers are considered to be new foragers and/or colony guards.