Nectar Foragers Research Articles

Learned olfactory cues affect pollen-foraging preferences in honeybees, Apis mellifera

Honeybees, Apis mellifera, show learned odour preferences for flowers that provide nectar as a reward. However, little is known about such behavioural plasticity when bees exploit pollen sources. Furthermore, the question about whether nectar and pollen foragers use the same learned strategy to improve foraging efficiency remains untested. Here, we demonstrate that honeybee foragers are able to learn odour cues associated with pollen as a reward. This was tested in free-flying bees in a dual-choice feeding device after the bees had gathered pollen from a scented feeder. Free-flying bees that associated odour with pollen successfully recalled these memories in olfactometer odour choice tests in a Y-maze, but they failed to show extension of the proboscis to learned odour cues when restrained (proboscis extension reflex, PER, assay). In addition, odour cues associated with pollen at the feeding site induced foraging reactivation when bees were blown into the hive. In PER assays, after fatty acids were applied to the bees’ antennae, pollen foragers were more responsive than nectar foragers. This, in turn, allowed pollen foragers in the PER assay to associate an odour cue with pollen in some trials. On the other hand, the unconditioned response (UR) and the odour-conditioned response (CR) to sucrose and amino acids were similar for both types of foragers. Pollen foragers also showed more URs to fresh pollen of different flower species and even performed better during conditioning with some pollen types as the reward than did nectar foragers. By studying biases in pollen-foraging responses after learning, we provide new insights to help comprehend and characterize the search for food between pollen and nonpollen honeybee foragers.

Ovarian regulation of foraging division of labour in Africanized backcross and pollen-hoarding honeybees

Division of labour (i.e. differential task performance) is the hallmark of social insects. One highly studied component of honeybee division of labour is foraging specialization through collection of protein (pollen) or carbohydrates (nectar). The reproductive ground plan hypothesis proposes that this foraging division of labour is regulated by the same physiological control networks that controlled foraging behaviour during the reproductive life cycle of solitary honeybee ancestors. Based on observed differences in foraging behaviour and reproductive anatomy between bees selected for storing high and low quantities of pollen (high and low pollen-hoarding strains) and observed differences between wild-type pollen and nectar foragers, the reproductive ground plan hypothesis suggests that ovary size in facultatively sterile worker honeybees has a regulatory effect on variation in foraging division of labour, with increased protein bias correlated with increased ovary size (measured as ovariole number). An alternative explanation for the link between ovary size and foraging behaviour is that genes for ovarian development and foraging are inherited together because of genetic linkage or chance gene associations in the selected and natural populations. To address this alternative explanation, we investigated the relationship between ovary size and foraging bias in honeybees where genetic linkage was broken using a backcross mating design. We also studied high- and low-strain bees where ovary size effects were partitioned from other potential linkage effects. We found that ovariole number was related to foraging bias in the backcross bees and in the selected strains, as predicted by the reproductive ground plan hypothesis. An interaction effect between nectar sugar concentration and ovariole number was observed in the backcross and high-strain bees. This result suggests a potential mechanism by which the ovary affects sucrose perception, which in turn influences foraging behaviour.

Temporal polyethism in Korean yellowjacket foragers, Vespula koreensis (Hymenoptera, Vespidae)

We examined the foraging behavior of the Korean yellowjacket, Vespula koreensis, to determine whether this species displays temporal polyethism. Using video-recordings of the entrances of artificial nest boxes installed in the field, we investigated the association between the tasks performed by workers and age. We identified three foraging tasks (pulp, nectar and prey foraging). Pulp foraging was performed by younger foragers, while nectar and prey foraging were performed by older foragers. We measured the foraging time (time spent outside of the nest during a single foraging bout) and the weight of the materials that foragers brought into the nest for each task to estimate the cost of the task. Pulp foraging was less costly than nectar or prey foraging by both measures. Taken together, the results suggest that yellowjacket foragers tend to perform low-cost task in their early foraging days and high-cost task later. Our results add to a growing literature showing temporal polyethism in social insects.

Pollination studies in large cardamom ( Amomum subulatum Roxb.) of Sikkim Himalayan region of India

Pollination studies in large cardamom were carried out at the research farm of ICAR Sikkim Centre, Gangtok, Sikkim, India during 2009–2010 to assess the effectiveness and efficiency of pollinators. Polleniferous flowers (65,890 ± 11,346.5 pollen/anther) of large cardamom produce spherical, large (108.64 μm × 96.32 μm) and echinate pollen with high pollen/ovule ratio (585.2 ± 134.8). Native bumblebee ( Bombus braviceps Smith.), a nectar forager, was identified as the most effective pollinator in terms of pollination potential index score (0.88), pollen removal (55.39%) and deposition rate (4.5%), pollination efficiency and pollen delivery mechanism whereas honey bee acted as a pollen robber. Flowers appeared to be generalized; however, functional specialization was exhibited indicating that only bumblebee is adaptable for pollination moreover, pollination mechanism was an indicative of “pollination syndrome”.

Pollen and ovule production, floral nectary structure, and nectar secretion dynamics in tristylous Lythrum salicaria L.

Lythrum salicaria L. (Lythraceae) is tristylous, each plant forming one of three floral morphs that differ in reciprocal placement of the stigma and two sets of anthers. Several reproductive traits were compared quantitatively among these morphs. Although mean pollen viability (≥93%) and total pollen per mature, indehiscent anther within a staminal level (mean CV = 11%) were constant, the patterns of mean pollen production per anther were complex, being significantly lowest in long stamens (1,490 grains) of the short-styled morph, but highest in intermediate stamens (3,590) of the long-styled morph. Overall, pollen production was greatest (38,200) in long-styled flowers and least (22,000) in short-styled ones. On the contrary, ovule quantities per ovary (mean 107) were similar among floral morphs; thus, pollen-to-ovule ratios spanned 192 (short-styled morph) to 364 (long-styled morph), relatively low values for a strictly xenogamous species. Each morph had a recessed annular nectary of similar dimensions encircling the ovary base, with equal numbers of modified stomata distributed uniformly on the nectary surface. Most stomata were solitary (94%), whereas 5% occurred in pairs and 1% of stomatal units had just one guard cell. During nectar secretion, about 16% of pores were closed plus 28% of pores were fully occluded. Similarly, nectar volumes and solute concentrations, peak rates of nectar secretion (mean 72–79 μg sugar h−1) at early afternoon, and the nectar’s sucrose prevalence [S/(G + F) ≥4.3] were not significantly different among morphs. Based on these similarities in nectary structure and nectar-secretion dynamics, traits rarely studied in tristylous species, the preferential visitation of any particular floral morph of L. salicaria during nectar foraging by insects is unlikely. Indeed, lack of discrimination among morphs by potential pollinators may be a key tenet of successful sexual reproduction in tristylous species.

Color vision and learning in the monarch butterfly,Danaus plexippus(Nymphalidae)

The monarch butterfly, Danaus plexippus, is well known for its intimate association with milkweed plants and its incredible multi-generational trans-continental migrations. However, little is known about monarch butterflies' color perception or learning ability, despite the importance of visual information to butterfly behavior in the contexts of nectar foraging, host-plant location and mate recognition. We used both theoretical and experimental approaches to address basic questions about monarch color vision and learning ability. Color space modeling based on the three known spectral classes of photoreceptors present in the eye suggests that monarchs should not be able to discriminate between long wavelength colors without making use of a dark orange lateral filtering pigment distributed heterogeneously in the eye. In the context of nectar foraging, monarchs show strong innate preferences, rapidly learn to associate colors with sugar rewards and learn non-innately preferred colors as quickly and proficiently as they do innately preferred colors. Butterflies also demonstrate asymmetric confusion between specific pairs of colors, which is likely a function of stimulus brightness. Monarchs readily learn to associate a second color with reward, and in general, learning parameters do not vary with temporal sequence of training. In addition, monarchs have true color vision; that is, they can discriminate colors on the basis of wavelength, independent of intensity. Finally, behavioral trials confirm that monarchs do make use of lateral filtering pigments to enhance long-wavelength discrimination. Our results demonstrate that monarchs are proficient and flexible color learners; these capabilities should allow them to respond rapidly to changing nectar availabilities as they travel over migratory routes, across both space and time.

Foraging Behaviour of Different Honeybees on Sunflower – A Comparative Study

Sunflower is a bee loving crop. The foraging behaviour of Apis dorsata L. was studied in comparison with Indian bee (A. cerana indica) and stingless bee (Trigona sp.) on this crop. A.dorsata outnumbered the other two bee species on capitulum after anther dehiscence during all the three stages of blooming. A. dorsata population varied at different hours of the day showing a bimodal distribution. The foragers were active from 10.00 to 11.00 am in the forenoon and 2.00 to 3.00 pm in the afternoon. Foraging behaviour showed distinct variation according to the floral reward collected. A.dorsata alone was found to tap the nectar fully due to its longer lapping tongue. Exclusive pollen collectors were rare. Majority of the foragers collected both pollen and nectar. Exclusive nectar foragers intentionally discarded the pollen load before final take off. Rains adversely affected the time of commencement and cessation of foraging. Among all the bee species studied, A.dorsata was the best pollinator of sunflower based on pollinator efficiency index. Wild honey bees like A.dorsata have to be conserved in crop ecosystem where planned pollination with hive bees is not in vogue.

Intelligent decisions from the hive mind: Foragers and nectar receivers of Apis mellifera collaborate to optimise active forager numbers

We present a differential equation-based mathematical model of nectar foraging by the honey bee Apis mellifera. The model focuses on two behavioural classes; nectar foragers and nectar receivers. Results generated from the model are used to demonstrate how different classes within a collective can collaborate to combine information and produce finely tuned decisions through simple interactions. In particular we show the importance of the ‘search time’ – the time a returning forager takes to find an available nectar receiver – in restricting the forager population to a level consistent with colony-wide needs.

Swarm-intelligent foraging in honeybees: benefits and costs of task-partitioning and environmental fluctuations

For honeybee colonies, it is crucial to collect nectar in an efficient way. Empiric experiments showed that the process of decision making, which allows the colony to select the optimal nectar source, is based on individual decisions. These decisions are made by returning nectar foragers, which alter their dancing behaviours based on the nectar source’s quality and based on the experienced search time for a receiver bee. Nectar receivers, which represent a shared limited resource for foragers, can modulate the foraging decisions performed by the colony. We investigated the interplay between foragers and receivers by using a multi-agent simulation. Therefore, we implemented agents which are capable of a limited set of behaviours and which spend energy according to their behaviour. In simulation experiments, we tested colonies with various receiver-to-forager ratios and measured colony-level results like the emerging foraging patterns and the colony’s net honey gain. We show that the number of receivers prominently regulates the foraging workforce. All tested environmental fluctuations are predicted to cause energetic costs for the colony. Task-partitioning additionally influences the colony’s decision-making concerning the question whether or not the colony sticks to a nectar source after environmental fluctuations.

An automated system for tracking and identifying individual nectar foragers at multiple feeders

Nectar-feeding animals have served as the subjects of many experimental studies and theoretical models of foraging. Their willingness to visit artificial feeders renders many species amenable to controlled experiments using mechanical “flowers” that replenish nectar automatically. However, the structural complexity of such feeders and the lack of a device for tracking the movements of multiple individuals have limited our ability to ask some specific questions related to natural foraging contexts, especially in competitive situations. To overcome such difficulties, we developed an experimental system for producing computer records of multiple foragers harvesting from simple artificial flowers with known rates of nectar secretion, using radio frequency identification (RFID) tags to identify individual animals. By using infrared detectors (light-emitting diodes and phototransistors) to activate the RFID readers momentarily when needed, our system prevents the RFID chips from heating up and disturbing the foraging behavior of focal animals. To demonstrate these advantages, we performed a preliminary experiment with a captive colony of bumble bees, Bombus impatiens. In the experiment, two bees were tagged with RFID chips (2.5 × 2.5 mm, manufactured by Hitachi-Maxell, Ltd., Tokyo, Japan) and allowed to forage on 16 artificial flowers arranged in a big flight cage. Using the resulting data set, we present details of how the bees increased their travel speed between flowers, while decreasing the average nectar crop per flower, as they gained experience. Our system provides a powerful tool to track the movement patterns, reward history, and long-term foraging performance of individual foragers at large spatial scales.

Sensory allometry, foraging task specialization and resource exploitation in honeybees

Insect societies are important models for evolutionary biology and sociobiology. The complexity of some eusocial insect societies appears to arise from self-organized task allocation and group cohesion. One of the best-supported models explaining self-organized task allocation in social insects is the response threshold model, which predicts specialization due to inter-individual variability in sensitivity to task-associated stimuli. The model explains foraging task specialization among honeybee workers, but the factors underlying the differences in individual sensitivity remain elusive. Here, we propose that in honeybees, sensory sensitivity correlates with individual differences in the number of sensory structures, as it does in solitary species. Examining European and Africanized honeybees, we introduce and test the hypothesis that body size and/or sensory allometry is associated with foraging task preferences and resource exploitation. We focus on common morphological measures and on the size and number of structures associated with olfactory sensitivity. We show that the number of olfactory sensilla is greater in pollen and water foragers, which are known to exhibit higher sensory sensitivity, compared to nectar foragers. These differences are independent of the distribution of size within a colony. Our data also suggest that body mass and number of olfactory sensilla correlate with the concentration of nectar gathered by workers, and with the size of pollen loads they carry. We conclude that sensory allometry, but not necessarily body size, is associated with resource exploitation in honeybees and that the differences in number of sensilla may underlie the observed differences in sensitivity between bees specialized on water, pollen and nectar collection.

Foraging Activity inPlebeia remota, a Stingless Bees Species, Is Influenced by the Reproductive State of a Colony

Colonies of the Brazilian stingless beePlebeia remotashow a reproductive diapause in autumn and winter. Therefore, they present two distinct reproductive states, during which colony needs are putatively different. Consequently, foraging should be adapted to the different needs. We recorded the foraging activity of two colonies for 30 days in both phases. Indeed, it presented different patterns during the two phases. In the reproductive diapause, the resource predominantly collected by the foragers was nectar. The majority of the bees were nectar foragers, and the peak of collecting activity occurred around noon. Instead, in the reproductive phase, the predominantly collected resource was pollen, and the peak of activity occurred around 10:00 am. Although the majority of the foragers were not specialized in this phase, there were a larger number of pollen foragers compared to the phase of reproductive diapause. The temperature and relative humidity also influenced the foraging activity.

The effect of foraging specialization on various learning tasks in the honey bee (Apis mellifera)

Honey bee foragers may collect nectar, pollen, water, or propolis, and their foraging specialization has been associated with several behavioral traits. By conditioning of the proboscis extension response (PER), we compared the performance of foragers that collected nectar, pollen, both nectar and pollen, or water in several learning and choice assays. Foragers were first tested in a three-trial olfactory associative learning assay. For further tests, we selected only good learners that responded in two out of three conditioning trials. One group was tested in an additional olfactory associative learning assay involving different reward volumes and concentrations. Another group was tested for risk sensitivity in a two-alternative forced-choice PER procedure and then in a latent inhibition (LI) assay. Levels of acquisition in olfactory associative learning were highest in pollen and water foragers, and better acquisition was associated with collection of heavier pollen loads and smaller and lighter nectar loads of lower sugar concentration. Among the good learners, pollen foragers still showed better acquisition than nectar foragers when rewarded with several volumes and concentrations of sucrose solution. Pollen and nectar foragers were equally risk averse, preferring a constant reward to a variable one, and choice was not affected by pollen load weight. Contrary to a previous study, pollen and nectar foragers were similarly affected by LI. We discuss possible explanations for the discrepancy between the two studies. Overall, our results suggest that differences between foraging groups in sensitivity to various stimuli may not correspond to differences in choice behavior.

Reappraising Social Insect Behavior through Aversive Responsiveness and Learning

BackgroundThe success of social insects can be in part attributed to their division of labor, which has been explained by a response threshold model. This model posits that individuals differ in their response thresholds to task-associated stimuli, so that individuals with lower thresholds specialize in this task. This model is at odds with findings on honeybee behavior as nectar and pollen foragers exhibit different responsiveness to sucrose, with nectar foragers having higher response thresholds to sucrose concentration. Moreover, it has been suggested that sucrose responsiveness correlates with responsiveness to most if not all other stimuli. If this is the case, explaining task specialization and the origins of division of labor on the basis of differences in response thresholds is difficult.MethodologyTo compare responsiveness to stimuli presenting clear-cut differences in hedonic value and behavioral contexts, we measured appetitive and aversive responsiveness in the same bees in the laboratory. We quantified proboscis extension responses to increasing sucrose concentrations and sting extension responses to electric shocks of increasing voltage. We analyzed the relationship between aversive responsiveness and aversive olfactory conditioning of the sting extension reflex, and determined how this relationship relates to division of labor.Principal FindingsSucrose and shock responsiveness measured in the same bees did not correlate, thus suggesting that they correspond to independent behavioral syndromes, a foraging and a defensive one. Bees which were more responsive to shock learned and memorized better aversive associations. Finally, guards were less responsive than nectar foragers to electric shocks, exhibiting higher tolerance to low voltage shocks. Consequently, foragers, which are more sensitive, were the ones learning and memorizing better in aversive conditioning.ConclusionsOur results constitute the first integrative study on how aversive responsiveness affects learning, memory and social organization in honeybees. We suggest that parallel behavioral modules (e.g. appetitive, aversive) coexist within each individual bee and determine its tendency to adopt a given task. This conclusion, which is at odds with a simple threshold model, should open new opportunities for exploring the division of labor in social insects.

Sucrose-response thresholds and the expression of behavioural tasks by middle-aged honeybee workers

Task assignment and division of labour in social groups persist as a key issue in the evolution of behaviour. Previous studies have argued that honeybees, Apis mellifera, display a pollen foraging syndrome that plays an important role in structuring the temporal division of labour within their colonies. Bees with low-sucrose-response thresholds early in life forage earlier and are more likely to be pollen-biased foragers than those that have higher thresholds early in life. We tested the hypothesis that sucrose-response thresholds are consistently expressed by bees performing a cluster of tasks—guarding, fanning and undertaking—that are typical of middle-aged bees. These three task groups show mean response thresholds that do not differ significantly from those of pollen foragers collected from the same colonies. However, a substantial percentage of undertakers do not respond in the bioassay, a feature that this group shares with nectar foragers. Notably, whereas mean colony response threshold varies among colonies, the ordination of response thresholds among tasks varies little among colonies. Sucrose-response thresholds for pollen and nectar foragers in our study were consistent with published results for these task groups. Our results support the hypothesis that task and sucrose-response thresholds are entwined and suggest the further hypothesis that fanning and guarding are associated with pollen collection.

Comportamento de <em>Apis mellifera</em> L. africanizada em flor de girassol (<em>Helianthus annuus</em> L.) e avaliação do desenvolvimento de uma colônia de <em>Apis mellifera</em> em área de girassol coberta

This research was carried out to evaluate the behavior of africanized honeybees, Apis mellifera L. (Hymenoptera, Apidae) and the development of a colony inside a covered area of sunflower, Helianthus annuus L. (Asteraceae) crop. It was used an area marked with 8 m x 3 m, and a second area in which a honeybee colony was installed inside a covered area with wire screen of 8m x 3m, two meters high in the highest part. The honeybees were constantly on sunflower during all day, however the Halictidae bees had been the most frequent in pollen harvesting, but these bees were seen until 11 a.m. In covered area, it occurred a reduction of 34.74% in swarm weight, 38.08% in honey, 100% in worker pupae, and 99.37% in egg-larvae. The honeybees gathered more nectar than pollen during the day. The nectar forager has more effect upon crop pollination than pollen foragers and pollen/nectar foragers, in sunflower.

Context- and scale-dependent effects of floral CO2 on nectar foraging by Manduca sexta.

Typically, animal pollinators are attracted to flowers by sensory stimuli in the form of pigments, volatiles, and cuticular substances (hairs, waxes) derived from plant secondary metabolism. Few studies have addressed the extent to which primary plant metabolites, such as respiratory carbon dioxide (CO(2)), may function as pollinator attractants. Night-blooming flowers of Datura wrightii show transient emissions of up to 200 ppm above-ambient CO(2) at anthesis, when nectar rewards are richest. Their main hawkmoth pollinator, Manduca sexta, can perceive minute variation (0.5 ppm) in CO(2) concentration through labial pit organs whose receptor neurons project afferents to the antennal lobe. We explored the behavioral responses of M. sexta to artificial flowers with different combinations of CO(2), visual, and olfactory stimuli using a laminar flow wind tunnel. Responses in no-choice assays were scale-dependent; CO(2) functioned as an olfactory distance-attractant redundant to floral scent, as each stimulus elicited upwind tracking flights. However, CO(2) played no role in probing behavior at the flower. Male moths showed significant bias in first-approach and probing choice of scented flowers with above-ambient CO(2) over those with ambient CO(2), whereas females showed similar bias only in the presence of host plant (tomato) leaf volatiles. Nevertheless, all males and females probed both flowers regardless of their first choice. While floral CO(2) unequivocally affects male appetitive responses, the context-dependence of female responses suggests that they may use floral CO(2) as a distance indicator of host plant quality during mixed feeding-oviposition bouts on Datura and Nicotiana plants.

Bees get a head start on honey production

Nectar concentration is assumed to remain constant during transport by honeybees between flowers and hive. We sampled crop contents of nectar foragers on Aloe greatheadii var. davyana, a major winter bee plant in South Africa. The nectar is dilute (approx. 20% w/w), but the crop contents of bees captured on flowers are significantly more concentrated. In returning foragers, the concentration increases further to 38-40%, accompanied by a volume decrease. The doubling of sugar concentration suggests that nectar is regurgitated onto the tongue and evaporated during foraging and on the return flight. Processing of the dilute nectar into honey thus begins early, aided by low ambient humidities. This has implications for honeybee thermoregulation, water balance and energetics during foraging, and for the communication of nectar quality to recruits.

Brain melatonin content and polyethism in adult workers of Apis mellifera and Apis cerana (Hym., Apidae)

Abstract: Radioimmunoassay showed that melatonin, N‐acetyl‐5‐methoxytryptamine, was synthesized in the brain of workers of Apis mellifera ligustica Spinola, and related to the polyethism of the workers. Statistically significant differences were found in melatonin levels between workers at different ages and between workers performing different tasks. The level in foragers was higher than that in young nurses. The highest melatonin level was found in 21‐day‐old adult workers (213.15 pg per worker head) and the lowest level in 1‐day‐old adult workers (6.08 pg per worker head); and the highest level in pollen‐collecting workers (404.13 pg per worker head) and the lowest in nurse workers (13.10 pg per worker head). Apis cerana cerana Fabricius showed a similar pattern, but the nectar foragers had the highest melatonin levels. The melatonin level also showed a daily rhythm. In 30‐day‐old adult workers there were two peaks, at 7:00 and 19:00 hours, and three troughs at 15:00, 21:00 and 1:00 hours respectively.

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

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