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.     

Thermoregulation of dancing bees: thoracic temperature of pollen and nectar foragers in relation to profitability of foraging and colony need

The thorax surface temperature of dancing honeybees (Apis mellifera carnica) recruiting nestmates to natural sources of nectar and pollen around Graz (Austria) was measured by real-time infrared thermography without touching them or disturbing social interactions. Thorax temperature during dancing was quite variable (31.4-43 degrees C). In the course of a foraging season it varied considerably and was always lower than in bees foraging from a highly profitable food source (2 molar sucrose 120 m from the hive). It averaged 38.0 degrees C (SD=2.24, n=224 dances) in the nectar foragers and 37.4 degrees C (SD=1.64, n=171) in the pollen foragers, resembling that of dancers foraging 0.5 molar sucrose from feeders with unlimited flow. Hive air temperature accounted only for about 3-8% of total variation. Foraging distance modulated dancing temperature in a way that, according to the decrease of the profitability of foraging with distance, maximum temperatures decreased and, in accordance with the increase of the dancing threshold with distance, minumum temperatures increased with distance, this way providing new support for the hypothesis that the dancing temperature is modulated by the profitability of foraging and the dancing and foraging motivation of the bees. Dancing temperature of both nectar and pollen dancers correlated with several parameters of the hive status, increasing with the amount of brood and decreasing with the amount of honey and pollen. These correlations are discussed with respect to literature reports on a colony's need for pollen and nectar, in particular the effect of brood and the amount of pollen on pollen foraging, and the effect of honey stores and demand for nectar on nectar foraging.     

Oxygen consumption in the foraging honeybee depends on the reward rate at the food source

Oxygen consumption of the honeybee Apis mellifera ligustica was measured as a function of the flow rate supply of sucrose solution at an automatic feeder located inside a respirometric chamber. Trained bees freely entered the respirometric chamber and collected the sucrose solution supplied. The mean value of the O₂ consumption rate per visit increased with the sucrose flow rate, and for a given flow rate, with increasing locomotor activity. However, when no locomotor activity was displayed, O₂ consumption also increased with increasing nectar flow rate. Crop load attained at the end of the visit showed a positive relationship with the nectar flow rate; however, for a given flow rate, O₂ consumption showed either no correlation or a negative one with the final crop load attained. It is concluded that the energy expenditure of the foraging bee is controlled by a motivational drive whose intensity depends on the reward rate at the food source. Accepted: 30 July 1996     

Relationship between respiratory pauses and heart rate during sleep in normal premature and full-term newborns

To investigate the relationship between central respiratory pauses and heart rate, we performed polygraphic recordings in 23 normal newborns (35 to 41 weeks conceptional age). We monitored the electroencephalogram, rapid eye movements, movements of the upper and lower limbs, chin and diaphragmatic electromyogram, electrocardiogram, thoracic and abdominal respiratory movements, air flow and transcutaneous PO2. Heart rate changes were analysed by computer measurement of R-R intervals and by cardiotachography. Respiratory pauses occurring after body movements and those not preceded by movements were studied separately. We analysed 1128 respiratory pauses greater than 3 s duration. No respiratory pause lasted more than 12 s. Independently of age, sleep state and respiratory pause duration, heart rate was significantly lower at the onset of respiratory pause, compared to control periods (selected away from the pause: 10 s before its onset and 20 s after its end). Heart rate slowed still further through the respiratory pause and reverted toward the baseline level after its end. When no movements preceded the respiratory pause, heart rate just before the pause was lower compared to control periods. These findings suggest the existence of simultaneous central commands responsible for both respiratory pause and heart rate deceleration.     

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.     

Ovarian control of nectar collection in the honey bee (Apis mellifera)

Honey bees are a model system for the study of division of labor. Worker bees demonstrate a foraging division of labor (DOL) by biasing collection towards carbohydrates (nectar) or protein (pollen). The Reproductive ground-plan hypothesis of Amdam et al. proposes that foraging DOL is regulated by the networks that controlled foraging behavior during the reproductive life cycle of honey bee ancestors. Here we test a proposed mechanism through which the ovary of the facultatively sterile worker impacts foraging bias. The proposed mechanism suggests that the ovary has a regulatory effect on sucrose sensitivity, and sucrose sensitivity impacts nectar loading. We tested this mechanism by measuring worker ovary size (ovariole number), sucrose sensitivity, and sucrose solution load size collected from a rate-controlled artificial feeder. We found a significant interaction between ovariole number and sucrose sensitivity on sucrose solution load size when using low concentration nectar. This supports our proposed mechanism. As nectar and pollen loading are not independent, a mechanism impacting nectar load size would also impact pollen load size.     

Correlation between octopaminergic signalling and foraging task specialisation in honeybees

Regulation of pollen and nectar foraging in honeybees is linked to differences in the sensitivity to the reward. Octopamine (OA) participates in the processing of reward-related information in the bee brain, being a candidate to mediate and modulate the division of labour among pollen and nectar foragers. Here we tested the hypothesis that OA affects the resource preferences of foragers. We first investigated whether oral administration of OA is involved in the transition from nectar to pollen foraging. We quantified the percentage of OA-treated bees that switched from a sucrose solution to a pollen feeder when the sugar concentration was decreased experimentally. We also evaluated if feeding the colonies sucrose solution containing OA increases the rate of bees collecting pollen. Finally, we quantified OA and tyramine (TYR) receptor genes expression of pollen and nectar foragers in different parts of the brain, as a putative mechanism that affects the decision-making process regarding the resource type collected. Adding OA in the food modified the probability that foragers switch from nectar to pollen collection. The proportion of pollen foragers also increased after feeding colonies with OA-containing food. Furthermore, the expression level of the AmoctαR1 was upregulated in foragers arriving at pollen sources compared with those arriving at sugar-water feeders. Using age-matched pollen and nectar foragers that returned to the hive, we detected an upregulated expression of a TYR receptor gene in the suboesophageal ganglia. These findings support our prediction that OA signalling affects the decision in honeybee foragers to collect pollen or nectar.     

Optimal foraging in bumblebees: Hunting by expectation

The foraging behaviour literature contains three hypotheses concerned with hunting by expectation. These suggest possible rules animals use to decide when to leave particular feeding sites and search in other places for food. Predictions of the three hypotheses were tested experimentally by varying the quality of plants (amount and distribution of nectar) encountered by bumblebees (Bombus appositus). Results support only a rate expectation hypothesis. Bees left multiflowered plants when the amount of nectar found in the first flower was below a threshold volume. Bees stayed on plants if they received greater than the threshold volume. This threshold nectar volume is close to the amount predicted if a bee forages to maximize its rate of net energy intake.     

The effect of genotype, age, sex, and caste on response thresholds to sucrose and foraging behavior of honey bees (Apis mellifera L.)

Bees derived from artificially selected high- and low-pollen-hoarding strains were tested for their proboscis extension reflex response to water and varying sucrose concentrations. High-strain bees had a lower response threshold to sucrose than low-strain bees among pre-foragers, foragers, queens and drones. Pre-foraging low-strain workers showed ontogenetic changes in their response threshold to sucrose which was inversely related to age. High-strain foragers were more likely to return with loads of water compared to low-strain foragers. Whereas low-strain foragers were more likely to return with loads of nectar. Low-strain nectar foragers collected nectar with significantly higher sucrose concentrations than did the high-strain nectar foragers. Alternatively, low-strain foragers were more likely to return empty compared to high-strain foragers. These studies demonstrate how a genotypically varied sensory-physiological process, the perception of sucrose, are associated with a division of labor for foraging. Accepted: 27 October 1998     

Modulation of sucrose response thresholds in honey bees (Apis mellifera L.): influence of genotype, feeding, and foraging experience

The perception of sugar is important to honey bees for making foraging decisions. We measured bees' perception by determining what concentration of sucrose touched to the antennae elicited the proboscis extension response (response threshold). A low response threshold (extension at low concentration) suggests a high perceptual value of sucrose. and vice versa. Perception of sucrose solutions differed between two artificially selected genotypic strains and was modulated by the bees' recent feeding experiences. Bees offered 10%, 30%, or 50% sucrose solutions in small cages overnight, and in large flight-cages or free-flying in the field for several days, had subsequent response thresholds positively correlated to the concentration offered. Empty bees, whether they were nectar, water or pollen foragers, dancers or non-dancers, had a significantly lower threshold than loaded bees. Crop volume affected response thresholds directly and independently of sucrose concentration. We interpret these findings as multiple mechanisms that operate in different time scales, modulating perception of sucrose. Changes occurred in the time scale of evolutionary processes as demonstrated by genotypic differences. Changes with foraging experience occur in hours or minutes while effects of crop filling are instantaneous.     

Effects of prey abundance on the foraging behaviour, diving efficiency and time allocation of breeding Guillemots Uria aalge

The foraging behaviour of Guillemots Uria aalge at sea was compared between 2 years of radically different food abundance. Radio telemetry was used to determine foraging locations and diving patterns. In the poor compared with the good food year, foraging trips were much longer, the birds foraged more than six times further from their breeding sites, they spent over five times as much time diving when at sea and their estimated energy expenditure was twice as great. Time spent foraging in the poor food year was at the expense of time spent sitting at the colony. The duration of a foraging trip was a poor indicator of distance travelled but a good indicator of the amount of time spent diving. Mean dive durations, surface pause durations and interbout periods did not differ between years, but individuals made more than four times as many dives per diving bout in the poor food year. Surface pause lengths did not vary with water depth in either year. In the poor food year, birds made shorter surface pauses for a dive of a gi^ven duration than in the good food year, possibly accepting a lactic acid debt in order to maximize searching time, The duration of the interbout period was positively related to the number of dives in the previous bout, and dives tended to get shorter in long diving sequences, suggesting possible exhaustion effects. These data demonstrate that breeding Guillemots have the capacity to adjust their foraging behaviour and time budgets in response to changes in food abundance, but this flexibility was not sufficient to compensate fully for the very low food abundance experienced by birds in this study.     

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.     

Foraging efficiency and size matching in a plant–pollinator community: the importance of sugar content and tongue length

A long‐standing question in ecology is how species interactions are structured within communities. Although evolutionary theory predicts close size matching between floral nectar tube depth and pollinator proboscis length of interacting species, such size matching has seldom been shown and explained in multispecies assemblages. Here, we investigated the degree of size matching among Asteraceae and their pollinators and its relationship with foraging efficiency. The majority of pollinators, especially Hymenoptera, choose plant species on which they had high foraging efficiencies. When proboscides were shorter than nectar tubes, foraging efficiency rapidly decreased because of increased handling time. When proboscides were longer than nectar tubes, a decreased nectar reward rather than an increased handling time made shallow flowers more inefficient to visit. Altogether, this led to close size matching. Overall, our results show the importance of nectar reward and handling time as drivers of plant–pollinator network structure.     

Scaling of nectar foraging in orchid bees

Morphology influences the rate at which foraging bees visit nectar flowers, the quantity of nectar they must consume to fuel their activities, and, consequently, the profitability of flower species. Because feeding time is a major determinant of visitation rate, I used a biomechanical model to examine how energy intake rate (E) varies with sucrose concentration, body mass (M), and proboscis length in orchid bees (Apidae: Euglossini). Under geometric scaling, the optimal sugar concentration (Smax) should be largely independent of body size, and E proportional to M1.0. In a comparative study of 30 orchid bee species ranging from 50 to 800 mg, Smax fell between 35% and 40% w/w, but E proportional to M0.54, significantly less than model predictions. Proboscis length and radius scale geometrically with body mass, but proboscis length exhibits substantial size-independent variation, particularly in small bees. One cost of a long proboscis is a reduction in both E and Smax in accordance with the scaling model. This finding highlights a difference between the lapping mechanism used by bumblebees and the suction mechanism used by orchid bees. A field study confirms that orchid bees harvest nectars with between 34% and 42% sucrose, independent of body size.     

Diving behaviour of guillemot Uria aalge, puffin Fratercula arctica and razorbill Alca tor da as shown by radio-telemetry

Information on dive and pause times and the numbers of dives in a sequence were obtained for six guillemots and single razorbill and puffin. There were marked differences in diving performance between the species with the order of ranking, in descending order of dive and pause duration, being guillemot, razorbill and puffin. For guillemots, 80% of dives were of 20–119 sec duration and 80% of pauses were 0–59 sec; the maximum dive lasted 202 sec. Puffin dives and pauses were much shorter, with 81% of dives lasting 0–39 sec and 95% of pauses being less than 20 sec, the longest dive was 115 sec. Comparisons of diving sequences made by the same individual indicated some flexibility in all aspects of the sequence but there were broad interspecific differences in the organization of the sequence. The puffin generally made a large number of relatively short dives separated by very short pauses which resulted in a high diving rate (1–5 dives/min) and the bird spending 78% of its time underwater. In contrast, guillemots had much shorter sequences with a few long dives and pauses and lower rates of diving (0–5-0-6 dives/min) and proportions of time underwater (61–65%). Guillemots and puffins may forage at different depths and have different foraging strategies.     

The effect of ambient humidity on the foraging behavior of the hawkmoth Manduca sexta

The foraging decisions of flower-visiting animals are contingent upon the need of an individual to meet both energetic and osmotic demands. Insects can alter their food preferences to prioritize one need over the other, depending on environmental conditions. In this study, preferences in nectar sugar concentrations (0, 12, 24 %) were tested in the hawkmoth Manduca sexta, in response to different levels of ambient humidity (20, 40, 60, and 80 % RH). Moths altered their foraging behavior when placed in low humidity environments by increasing the volume of nectar imbibed and by consuming more dilute nectar. When placed in high humidity environments the total volume imbibed decreased, because moths consumed less from dilute nectars (water and 12 % sucrose). Survivorship was higher with higher humidity. Daily foraging patterns changed with relative humidity (RH): moths maximized their nectar consumption earlier, at lower humidities. Although ambient humidity had an impact on foraging activity, activity levels and nectar preferences, total energy intake was not affected. These results show that foraging decisions made by M. sexta kept under different ambient RH levels allow individuals to meet their osmotic demands while maintaining a constant energy input.     

Cerebellar Nuclear Neurons Use Time and Rate Coding to Transmit Purkinje Neuron Pauses

Neurons of the cerebellar nuclei convey the final output of the cerebellum to their targets in various parts of the brain. Within the cerebellum their direct upstream connections originate from inhibitory Purkinje neurons. Purkinje neurons have a complex firing pattern of regular spikes interrupted by intermittent pauses of variable length. How can the cerebellar nucleus process this complex input pattern? In this modeling study, we investigate different forms of Purkinje neuron simple spike pause synchrony and its influence on candidate coding strategies in the cerebellar nuclei. That is, we investigate how different alignments of synchronous pauses in synthetic Purkinje neuron spike trains affect either time-locking or rate-changes in the downstream nuclei. We find that Purkinje neuron synchrony is mainly represented by changes in the firing rate of cerebellar nuclei neurons. Pause beginning synchronization produced a unique effect on nuclei neuron firing, while the effect of pause ending and pause overlapping synchronization could not be distinguished from each other. Pause beginning synchronization produced better time-locking of nuclear neurons for short length pauses. We also characterize the effect of pause length and spike jitter on the nuclear neuron firing. Additionally, we find that the rate of rebound responses in nuclear neurons after a synchronous pause is controlled by the firing rate of Purkinje neurons preceding it.     

Nectar foraging behaviour is affected by ant body size in Camponotus mus

The nectivorous ant Camponotus mus shows a broad size variation within the worker caste. Large ants can ingest faster and larger loads than small ones. Differences in physiological abilities in fluid ingestion due to the insect size could be related to differences in decision-making according to ant size during nectar foraging. Sucrose solutions of different levels of sugar concentration (30% or 60%w/w), viscosity (high or low) or flow rate (ad libitum or 1microl/min) were offered in combination to analyse the behavioural responses to each of these properties separately. Differences were found depending on ant body size and the property compared. A regulated flow produced smaller crop loads for medium and large ants compared to the same solution given ad libitum. All foragers remained longer times feeding at the regulated flow source but larger ants often made longer interruptions. When sugar concentration was constant but viscosity was high, only large ants increased feeding time. Constant viscosity with different sugar concentration determined longer feeding time and bigger loads for the most concentrated solution for small but not for large ants. Small ants reached similar crop loads in a variety of conditions while large ants did not. These differences could be evidence of a possible specialization for nectar foraging based on ant body size.     

Honeybees and the nectar of Echium plantagineum L. in southeastern Australia

An account is given of the flower of Echium plantagineum in south-eastern Australia, including stages and timing of flowering, behaviour of raindrops in the flower and aspects of floral microclimate. The concentration of nectar solutes varied with time and site, with means varying from 2 to 62% (as g sucrose/100 g solution). There was a significant negative correlation between nectar solute concentration and ambient relative humidity: the drier the air, the more concentrated the nectar. Rates of nectar secretion per flower varied with the bagging method, with long-term bagging reducing net secretion rates, possibly because of re-absorption. Rates varied with time, day and site, with a temporal pattern of change suggesting a link between rates of photosynthesis and secretion. Maximum nectar secretion rates in short-term bagging experiments were ca. 300 μg sugar/flower/hr (equivalent to > 2 mglflower/24 hr). Secretion rate was correlated with flower density. As flower density increased, secretion rate per flower decreased; rate of sugar production per unit area increased relatively more slowly than flower density. E. plantagineum could produce > 500 mg sugar/m²/day. Honeybees foraged on E. plantagineum only at ambient air temperatures above ca. 17°C unless irradiance exceeded ca. 750 W m^-2. Foragers collected nectar or pollen alone, or both, with the type of visit significantly correlated with nectar solute concentration. Below 35% (as g sucrose/100 g solution) most bees took pollen only; above 40%, most took nectar. Mean standing crop of nectar was generally < 100 μg/flower when most bees were taking nectar, but could exceed 1000 μg/flower when bees were absent or foraging mainly for pollen. Honeybees did not always remove all nectar from flowers they probed. Reabsorption of residual nectar may augment the following day's secretion.