Assessment of food source profitability in honeybees (<Emphasis Type="Italic">Apis mellifera</Emphasis>): how does disturbance of foraging activity affect trophallactic behaviour?

When forager honeybees (Apis mellifera) return to the hive after a successful foraging trip, they unload the collected liquid to recipient hive mates through mouth-to-mouth contacts (trophallaxis). The speed at which the liquid is transferred (unloading rate) from donor to recipient is related to the profitability of the recently visited food source. Two main characteristics that define this profitability are the flow of solution delivered by the feeder and the time invested by the forager at the source (visit time). To investigate the effect of visit time on trophallactic behaviour, donor foragers were trained to a rate feeder that could deliver different flows of solution. We dissociated visit time and flow of solution by introducing pauses in the solution's deliverance at different moments of the foraging visit. We analysed whether timing of the non-deliverance period within the visit is important for the forager's assessment of resource profitability. During the subsequent trophallactic encounter with a hive mate, unloading rate was related to the total time invested by the forager at the food source only if the ingestion process had already been started. These results together with previous ones suggest that foragers integrate an overall flow rate of solution of the feeder throughout the entire foraging visit.     

Trophallaxis in honeybees, Apis mellifera (L.), as related to their past experience at the food source

Forager honeybees returning to the hive after a successful foraging trip unload the collected liquid to recipient hivemates through mouth-to-mouth food exchange contacts (trophallaxis). The speed at which the liquid is transferred (unloading rate) from donor to recipient is related to the profitability offered by the recently visited food source. However, because a forager's evaluation of the profitability of a food source, as measured by dancing behaviour, is influenced by previous foraging experience, we investigated whether trophallaxis might also be influenced by previous foraging experience. We measured unloading rate for a given profitability condition at the food source (in terms of solution flow rate) in three groups of foragers that differed in their previous experience at the source. One group experienced the same flow rate of solution in five successive visits (control group), another group experienced a lower flow rate in the first four visits and the third group experienced a higher flow rate in the first four visits. The results of the present study show that animals trained to a lower flow rate increased their unloading rate compared with the control group, indicating an influence of past foraging experience on their evaluation of food source profitability. This influence was not observed in the group trained to a higher flow rate, which responded as the control group. Additional experiments indicated that foragers appear to evaluate the profitability of the source by integrating an overall flow rate throughout the entire visit, instead of measuring only the current flow rate delivered by the feeder. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

Descriptive study of antennation during trophallactic unloading contacts in honeybees <Emphasis Type="Italic">Apis mellifera carnica</Emphasis>

Summary  Trophallaxis, the mouth-to-mouth transfer of food, is a widespread behavior occurring between individuals of eusocial insect societies. Antennal movements during food transfer are, in honeybees, too rapid to be characterized using standard video recordings. Using a high-speed camera (200 frames/s), we recorded nectar unloading performed by forager honeybees (Apis mellifera carnica Spinola) within the hive once they returned from collecting sugar solution at a feeder that delivered nectar at a variable rate. Frequency patterns attained a mean value of 13 Hz. Antennation intensity showed a tendency to increase with the reward rate recently exploited by the food donor. This raises the question whether or not antennation intensity is a reliable parameter providing modulatory information related to food-source profitability.Received 12 September 2002; revised 21 March 2002; accepted 24 April 2003.     

Trophallaxis in the honeybee Apis mellifera (L.): the interaction between flow of solution and sucrose concentration of the exploited food sources

Forager bees arriving at the hive after visiting a nectar source, unload the collected liquid food to recipient hivemates through mouth-to-mouth contact (trophallaxis). We analysed whether the main characteristics that define nectar in energetic terms, that is, rate of production (flow of solution), sucrose concentration and rate of sucrose production (sucrose flow) influence trophallactic behaviour. Individual bees trained to feed at a regulated-flow feeder offering sucrose solution were captured once the foraging visit was complete and placed in an acrylic arena with a recipient bee that had not been fed. The rate at which liquid was transferred during the subsequent trophallactic contact (transfer rate) was analysed as a function of the different solution flows and sucrose concentrations offered at the feeder. A relationship was found between transfer rate during trophallaxis and the flow of solution previously presented at the feeder. This relationship was independent of sucrose concentration when above a certain threshold value (ca. 22% weight on weight). We also analysed whether the rate of sucrose deliverance of the food source (sucrose flow) influenced the rate at which the solution was transferred. No clear relationship was found between the rate of sucrose deliverance during trophallactic events (sucrose transfer rate) and the sucrose flow presented at the feeder. The possibility that trophallaxis could be a communication channel through which quantitative information on food source profitability is transmitted among hivemates is discussed. Copyright 2000 The Association for the Study of Animal Behaviour.     

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.     

Persistence to Unrewarding Feeding Locations by Honeybee Foragers (Apis mellifera): the Effects of Experience,Resource Profitability and Season

Honeybee foragers that find a profitable food source quickly establish spatiotemporal memories, which allow them to return to this foraging site on subsequent days. The aim of this study was to investigate how the previous experience of honeybee foragers at a feeding location affects their persistence at that location once food is no longer available. We hypothesised that persistence would be greater to locations that were more rewarding (closer to the hive, higher concentration of sucrose solution), for which a bee had greater prior experience (0.5‐h vs. 2‐h training access), and at times of the year of lower nectar availability in the environment. We studied individually marked worker bees from four colonies trained to sucrose‐solution feeders. Our results support most of these predictions. Persistence, measured both in duration and number of visits, was greater to locations that previously offered sucrose solution of higher concentration (2 m vs. 1 m ) or were closer to the hive (20 m vs. 450 m). Persistence was also greater in bees that had longer access at the feeder before the syrup was terminated (2 h vs. 0.5 h). However, contrary to our prediction, persistence was not higher in the season of the lowest nectar availability in the environment in the study year. In summary, honeybees show considerable persistence at foraging sites that ceased providing rewards. The decision to abandon a foraging site depends on the profitability the forager experienced when the foraging site was still rewarding.     

Changes in food source profitability affect Nasonov gland exposure in honeybee foragers Apis mellifera L.

Summary. When arriving at a known artificial food source, foraging honeybees usually perform circular flights around the feeding place prior to landing. During these flights bees expose their Nasonov gland, an exocrine gland located at the base of the 7^th tergum, that releases a complex blend of volatiles. This behavior may continue even after the bee starts food ingestion. The proportion of bees exposing the Nasonov gland and the duration of its exposure before and during feeding for individual bees were quantified. Trained bees collected sugar solution during 12 visits from a feeder located at 160 m from the hive. Five different reward programs were presented: three constant and two variable. The constant programs offered 0.6, 1.2 or 2.4 M sugar for all 12 visits, while the variable programs delivered either 0.6, 1.2, 0.6 M or 0.6, 2.4, 0.6 M, four visits for each molarity. Results showed that sugar concentration changed the thresholds and durations of Nasonov gland exposure. However, this relationship was found only for Nasonov exposure before bees began to feed. During feeding, a protruded Nasonov gland was only observed for bees that had exposed it prior to feeding; suggesting that Nasonov gland exposure before feeding is a releaser of the during-feeding exposure. In variable reward programs, changes in sugar concentration were followed by changes in both thresholds and durations of exposure. However, Nasonov gland exposure during feeding did not appear to decrease based on measurements of the low profitability during the current foraging visit. These results suggest that Nasonov gland exposure is programmed on the basis of reward expectations, with the bees having acquired this information in the previous foraging visits to the food source.     

Metabolic rate during foraging in the honeybee

Summary The metabolic rate of free-flying honeybees, Apis mellifera ligustica, was determined by means of a novel respirometric device that allowed measurement of CO₂ produced by bees foraging under controlled reward at an artificial food source. Metabolic rate increased with reward (sugar flow rate) at the food source. In addition, there was no clear-cut dependence of metabolic rate on load carried during the visit, neither as crop load nor as supplementary weights attached to the thorax. The hypothesis that metabolic rate, as well as foraging and recruiting activities, depend on the motivational state of the foraging bee determined by the reward at the food source is discussed.Abbreviations CL crop load (fuel load at the FSS) - FC (=CL-W_c), fuel consumed during the visit - FSS food source simulator - FSS +dome, respirometric chamber - NVT non-visit time - TT titration time - VT visit time - W_c (=W_f-W_i) load carried at the end of the visit - W_f final weight of the forager - W_i initial weight of the forager     

Foraging pauses and their meaning as an economic strategy in the honeybee Apis mellifera L.

When conditioned honeybees collect sucrose solution delivered at a range of low-profit flow rates for the hive, they increase the pause length between successive visits. If sucrose solution was delivered continuously, it accumulated at the food source in an amount proportional to the pause length and the flow rate of nectar. When the flow rate of sucrose solution was further decreased but kept constant throughout the day, a threshold level was attained in which oscillations in the length of the pauses were observed. The relationship between the amount of accumulated nectar and subsequent pause length at this threshold level can be depicted by means of a power function. The best fit allowed the calculation of the values of parameters that quantitatively describe the control system regulating foraging activity. The importance of foraging pauses as a strategy to cope with changing nectar availability is discussed. Accepted: 7 January 1998     

Flower choice in honeybees: Effects of food value and flower density

To test the effects of food value on the flower choice, individual honeybees (Apis mellifera) were offered a choice of 25 % sucrose solution (SS) and 1 of 6 different SSs, ranging from 5 % to 50 % SS, at either a low or a high flower density. Artificial flowers were filled with each SS. The honeybees showed a stronger preference for a concentrated SS to a diluted SS at a high than at a low flower density, and the degree of preference was positively correlated to the difference in the sucrose concentration between paired SSs. These foraging patterns were consistent with qualitative predictions from optimal foraging theory. Furthermore, it was found that experience in feeding on a concentrated SS lowered the foraging motivation for a diluted SS at the high flower density, but not at the low flower density. I discuss the effects of food density, food profitability and experience on the foraging behaviour of honeybees.     

Individual recruitment in honeybees, <Emphasis Type="Italic">Apis mellifera</Emphasis> L.

The recruitment of honeybee foragers individually exploiting a low-flow rate-feeder that presented different temporal reward programs was experimentally analyzed. By capturing hive bees that landed at the feeder in a 2-h period, the arrival rate of incoming bees could be obtained. With this procedure we quantitatively analyzed the maximum number of hive bees that can be brought to the feeding station by single foragers. Test bees collected sucrose solution during 12 visits to a rate-feeder located 160 m from the hive. The constant programs offered 0.6, 1.2, or 2.4 M sugar for all 12 visits, while the variable programs delivered either 0.6, 1.2, or 0.6 M or 0.6, 2.4, or 0.6 M, with four visits for each molarity. Results showed that the sucrose concentration exploited by single foragers increased the arrival rate. Moreover, there was a linear relationship within this range of sucrose concentrations that presented a slope of 1.58. Since the sugar solutions were provided at the same flow rate (5 μl/min) in all the programs, the arrival rate expressed in terms of sucrose flow rate (milligrams of sucrose/minute) shows that one additional incoming bee per hour arrived when the single forager assessed an increase in the sucrose flow rate of 0.75 mg sucrose/min at the rate-feeder. The absence of differences in the frequency of visits of the single foragers during the constant programs suggests that the differences observed in the arrival rate can mainly be explained by a more intensive display of the recruitment mechanisms performed per foraging trip instead of by their iterativeness throughout different foraging cycles. Variable reward programs showed that arrival rate is rapidly adjusted according to the reward change and is independent of its magnitude. Received in revised form: 17 August 2001 Electronic Publication     

Temperature and forager body size affect carbohydrate collection in German yellowjackets, Vespula germanica (Hymenoptera, Vespidae)

The classic formulation of optimal foraging theory predicts that a central-place forager will gather more food if it is required to travel farther from the nest to find that food. We examined the foraging behavior of German yellowjackets (Vespula germanica) to determine whether carbohydrate foragers follow this pattern. We trained foragers to collect 2 M fructose solution at 5 or 50 m from the nest and measured the time spent feeding, load size, and the rate of delivery. We show that as a forager’s crop fills during a foraging bout, the amount of solution ingested per second decreased. However, load size did not change as wasps collected food up to 50 m from the nest. Instead, temperature and body size were better predictors of the volume of fructose a forager carried. Finally, the rate of fructose delivered to the nest was higher at warmer temperatures. Due to the fact that wasps gather more food but feed for shorter periods of time at warmer temperatures, we found an overall negative relationship between feeding time and load size. We conclude that the strong effects temperature had on the behavior of V. germanica foragers imply that feeding time may not always be an accurate predictor of the size of the load an individual carries back to the nest. Results from this study suggest that in yellowjacket colonies, foragers can collect and bring disproportionately more food back to the nest during the warmest days of the summer, a time of year when this pest species reaches peak population size during its annual colony cycle.     

The control of the proventriculus in the honeybee (Apis mellifera carnica L.) I. A dynamic process influenced by food quality and quantity?

The control of crop emptying in foraging honeybees was investigated in individuals trained to collect defined amounts of sugar solutions. Following feeding, they were dissected after fixed periods of time in order to measure crop content and haemolymph sugar titers. Between feeding and dissection, the metabolic rate of every investigated forager was measured using open-flow respirometry, so as to assess the effects of both food quality (concentration, molarity and viscosity of the fed sugar solution) and food quantity on the transport rate through the proventriculus. The sugar transport rate through the proventriculus was observed to be mainly dependent on the metabolic expenditure of the individual. Bee foragers were able to precisely adjust the sugar transport rate to their metabolic rates, but under certain conditions, an excess of sugars was transported through the proventriculus, more than needed to cover the bee’s energetic demands. This excess depended on the nutritive value and quantity of the fed sugar solution, and on the time after feeding. It did not depend on the metabolic rate of the bee, the molarity, or the viscosity of the fed sugar solution. As long as the bees did not exhaust their crop contents, the haemolymph sugar titers were unaffected by this excess amount transported, by the time after feeding, the concentration and the viscosity of the fed sugar solution. For all feeding conditions assayed, the haemolymph trehalose titer remained constant, while the titers of other haemolymph sugars varied. It is suggested that the trehalose concentration in the haemolymph is regulated in honeybees, and that it represents the controlled variable in the feedback loop responsible for the transport rate through the proventriculus.     

Allocation of Colony‐Level Foraging Effort in Vespula germanica in Response to Food Resource Quantity,Quality, and Associated Olfactory Cues

In social insects, selection takes place primarily at the level of the colony. Therefore, unlike solitary insects, social species are expected to forage at rates that maximize colony fitness rather than individual fitness. Workers can increase the net benefit of foraging by responding to increased resource availability, by responding more strongly to higher‐quality resources, and by decreasing the uncertainty with which nestmates find resources. Unlike many ants and social bees, no social wasp is known to utilize a nest‐based recruitment signal to inform nestmates of food location. On the other hand, wasps do learn the odor of food brought to the nest and use this cue to locate the food source outside the nest. Here, we quantify the effects of three food‐associated variables on the allocation of foraging effort in the yellowjacket Vespula germanica. We used an experimental approach to assess whether resource quantity, quality, or associated olfactory information affect the probability that a forager will leave the nest on a foraging trip. We addressed these questions by inserting a known amount of sucrose solution directly into nests and recording foraging effort (departure rate) over the subsequent hour‐long observation period. No differences were found in foraging effort because of the presence/absence of olfactory cues, but there was strong evidence that foraging effort increased in response to resource influx and resource quality. Thus, while olfactory cues are learned in the nest, only resource quality and the cue of increased amount of food in the nest factor into a forager's decision of whether or not to depart on a foraging trip. However, as prior work has shown, once a wasp forager leaves the nest, it uses the learned olfactory cues to aid in finding resources.     

Bumble bee olfactory information flow and contact-based foraging activation

Nestmate foraging activation and interspecific variation in foraging activation is poorly understood in bumble bees, as compared to honey bees and stingless bees. We therefore investigated olfactory information flow and foraging activation in the New World bumble bee species, Bombus impatiens. We (1) tested the ability of foragers to associate forager-deposited odor marks with rewarding food, (2) determined whether potential foragers will seek out the food odor brought back by a successful forager, and (3) examined the role of intranidal tactile contacts in foraging activation. Bees learned to associate forager-deposited odor marks with rewarding food. They were significantly more attracted to an empty previously rewarding feeder presented at a random position within an array of eight previously non-rewarding feeders. However, foragers did not exhibit overall odor specificity for short-term, daily floral shifts. For two out of three tested scents, activated foragers did not significantly prefer the feeder providing the same scent as that brought back by a successful forager. Finally, bees contacted by the successful forager inside the nest were significantly more likely to leave the nest to forage (38.6% increase in attempts to feed from empty feeders) than were non-contacted bees. This is the first demonstration that tactile contact, a hypothesized evolutionary basal communication mechanism in the social corbiculate bees, is involved in bumble bee foraging activation. Received 4 September 2007; revised 30 May 2008; accepted 15 July 2008.     

The short-term regulation of foraging in harvester ants

In the seed-eating ant Pogonomyrmex barbatus, the return ofsuccessful foragers stimulates inactive foragers to leave thenest. The rate at which successful foragers return to the nestdepends on food availability; the more food available, the morequickly foragers will find it and bring it back. Field experimentsexamined how quickly a colony can adjust to a decline in therate of forager return, and thus to a decline in food availability,by slowing down foraging activity. In response to a brief, 3-to 5-min reduction in the forager return rate, foraging activityusually decreased within 2–3 min and then recovered within5 min. This indicates that whether an inactive forager leavesthe nest on its next trip depends on its very recent experienceof the rate of forager return. On some days, colonies respondedmore to a change in forager return rate. The rapid colony responseto fluctuations in forager return rate, enabling colonies toact as risk-averse foragers, may arise from the limited intervalover which an ant can track its encounters with returning foragers.     

Sticking to their choice – honey bee subfamilies abandon declining food sources at a slow but uniform rate

Abstract. 1. The allocation of honey bee foragers among food patches is a result of decisions made by individual bees that are based on internal and external cues.
2. Decision-making processes are often based on internal thresholds. For example, if the quality of the food source is assessed by a forager as exceeding its internal threshold, the bee will continue foraging on that food source.
3. It is often assumed that all individuals have the same threshold and therefore use the same thresholds in decision-making, but because the honey bee queen mates with 12–30 males, the workers within a colony are genetically heterogeneous. Thus, the thresholds used by individual bees may be genetically variable within a colony.
4. Models of colony-level foraging behaviour of honey bees suggest that the rate of abandoning food sources is a critical parameter affecting foraging success. Moreover, these models show that variance among subfamilies in their abandonment rates may increase the colony's foraging efficiency.
5. Experimental data showing the relationship between the probability of abandoning a food source and its profitability are lacking, as is information on any variation in abandonment rates among subfamilies.
6. Abandonment rates were determined experimentally for four honey bee families for seven different sucrose concentrations. The results showed that abandonment rates appear to be invariant among (sub)families. The importance of forager fidelity to declining food sources is discussed with respect to foraging efficiency in a changing environment.     

Optic flow informs distance but not profitability for honeybees

How do flying insects monitor foraging efficiency? Honeybees (Apis mellifera) use optic flow information as an odometer to estimate distance travelled, but here we tested whether optic flow informs estimation of foraging costs also. Bees were trained to feeders in flight tunnels such that bees experienced the greatest optic flow en route to the feeder closest to the hive. Analyses of dance communication showed that, as expected, bees indicated the close feeder as being further, but they also indicated this feeder as the more profitable, and preferentially visited this feeder when given a choice. We show that honeybee estimates of foraging cost are not reliant on optic flow information. Rather, bees can assess distance and profitability independently and signal these aspects as separate elements of their dances. The optic flow signal is sensitive to the nature of the environment travelled by the bee, and is therefore not a good index of flight energetic costs, but it provides a good indication of distance travelled for purpose of navigation and communication, as long as the dancer and recruit travel similar routes. This study suggests an adaptive dual processing system in honeybees for communicating and navigating distance flown and for evaluating its energetic costs.     

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.     

Time constraint on food choice in provisioning blue tits, Parus caeruleus: the relationship between feeding rate and prey size

Previous work on food-provisioning behaviour in blue tits suggested that the parents could gather larger prey items only by making longer foraging excursions, for example, by being more selective or by reaching more distant (and less exploited) feeding sites. Here, I show that within-nest, within-day variation in size of prey delivered by the parent could be explained by the time since its last visit. In unmanipulated conditions, size of larvae tended to increase with the time spent away from the nest. A significant positive relationship was more likely at high provisioning rates, suggesting that periods of intense feeding limited the size of prey delivered to the brood. To assess the effect of less intense feeding on prey size, I experimentally increased food availability to the tits. The parents could decide whether to eat the extra food or feed it to the nestlings. In both cases, food supplementation could result in longer time lags between natural feedings. Food-supplemented parents consumed the extra food and fed it to their nestlings, made longer foraging trips and delivered larger natural larvae than controls. In this group, size of larvae was more constant during the observation period and was independent of the time since the parent's last visit. This suggests that, below some value of visit rate, prey size is no longer limited by the duration of the foraging trip. The results support the view that tits continually vary visit rate and prey size. There is some evidence that these adjustments are made by changing food selectivity in response to changes in the state of the brood and of the parents.Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved .