The role of the vibration signal in the house-hunting process of honey bee (<Emphasis Type="Italic">Apis mellifera</Emphasis>) swarms

The function of the vibration signal of the honey bee (Apis mellifera) during house hunting was investigated by removing vibrating bees from swarms and examining the effects on waggle dancing for nest sites, liftoff preparations and swarm movement. We compared house hunting among three swarm types: (1) test swarms (from which vibrating bees were removed), (2) manipulated control (MC) swarms (from which randomly selected workers and some waggle dancers were removed), and (3) unmanipulated control (UC) swarms (from which no bees were removed). The removal of vibrating bees had pronounced effects on liftoff preparations and swarm movement. Compared to the MC and UC swarms, the test swarms had significantly greater liftoff-preparation periods, were more likely to abort liftoff attempts, and in some cases were unable to move to the chosen site after the swarm became airborne. However, the three swarm types did not differ in overall levels of waggle dance activity, the time required to achieve consensus for a nest site, the rate at which new waggle dancers were recruited for the chosen site, or the ability to maintain levels of worker piping necessary to prepare for flight. The removal of vibrating bees may therefore have altered liftoff behavior because of a direct effect on vibration signal activity. A primary function of the signal during house hunting may be to generate a level of activity in workers that enhances and coordinates responses to other signals that stimulate departure and movement to a new location.Communicated by R. Page     

Worker piping in honey bees (<Emphasis Type="Italic">Apis mellifera</Emphasis>): the behavior of piping nectar foragers

This study investigates the brief piping signals ("stop signals") of honey bee workers by exploring the context in which worker piping occurs and the identity and behavior of piping workers. Piping was stimulated reliably by promoting a colony's nectar foraging activity, demonstrating a causal connection between worker piping and nectar foraging. Comparison of the behavior of piping versus non-piping nectar foragers revealed many differences, e.g., piping nectar foragers spent more time in the hive, started to dance earlier, spent more time dancing, and spent less time on the dance floor. Most piping signals (approximately 99%) were produced by tremble dancers, yet not all (approximately 48%) tremble dancers piped, suggesting that the short piping signal and the tremble dance have related, but not identical, functions in the nectar foraging communication system. Our observations of the location and behavior of piping tremble dancers suggest that the brief piping signal may (1) retard recruitment to a low-quality food source, and (2) help to enhance the recruitment success of the tremble dance.     

The occurrence and context of tremble dancing in free-foraging honey bees (<Emphasis Type="Italic">Apis mellifera</Emphasis>)

Nectar foraging in honey bees is regulated by several communication signals that are performed mainly by foragers. One of these signals is the tremble dance, which is consistently performed by foragers from a rich food source which, upon return to the hive, experience a long delay before unloading their nectar to a nectar receiver. Although tremble dancing has been studied extensively using artificial nectar sources, its occurrence and context in a more natural setting remain unknown. Therefore, this study tests the sufficiency of the current explanations for tremble dancing by free-foraging honey bees. The main finding is that only about half of the observations of tremble dancing, referred to as delay-type tremble dancing, are a result of difficulty in finding a nectar receiver. In the remaining observations, tremble dancing was initiated immediately upon entering the hive, referred to as non-delay-type tremble dancing. Non-delay tremble dancing was associated with first foraging successes, both in a forager's career and in a single day. More than 75% of tremble dancing was associated with good foraging conditions, as indicated by the dancer continuing to forage after dancing. However, at least some of the other cases were associated with deteriorated foraging conditions, such as the end of the day, after which foraging was discontinued. No common context could be identified that explains all cases of tremble dancing or the subset of non-delay-type tremble dancing. This study shows that the current explanations for the cause of the tremble dance are insufficient to explain all tremble dancing in honey bees that forage at natural food sources.     

The effects of young brood on the foraging behavior of two strains of honey bees (<Emphasis Type="Italic">Apis mellifera</Emphasis>)

Honey bee foragers specialize on collecting pollen and nectar. Pollen foraging behavior is modulated by at least two stimuli within the nest: the presence of brood pheromone and young larvae and the quantity of stored pollen. Genetic variation in pollen foraging behavior has been demonstrated repeatedly. We used selected high and low pollen-hoarding strains of bees that differ dramatically in the quantity of pollen collected to determine if the observed differences in foraging could be explained by differential responses to brood stimuli. Workers from the high and low pollen-hoarding strains and wild-type bees were co-fostered in colonies with either brood or no brood. As expected based on previous studies, returning high pollen-hoarding foragers collected heavier pollen loads and lighter nectar loads than low pollen-hoarding bees. Effects of brood treatment were also observed; bees exposed to brood collected heavier pollen loads and initiated foraging earlier than those from broodless colonies. More specifically, brood treatment resulted in increased pollen foraging in high pollen-hoarding bees but did not affect pollen foraging in low pollen-hoarding bees, suggesting that high pollen-hoarding bees are more sensitive to the presence of brood. However, response to brood stimuli does not sufficiently explain the differences in foraging behavior between the strains since these differences persisted even in the absence of brood.     

Intracolonial genetic diversity in honeybee (<Emphasis Type=Italic>Apis mellifera</Emphasis>) colonies increases pollen foraging efficiency

Multiple mating by honeybee queens results in colonies of genotypically diverse workers. Recent studies have demonstrated that increased genetic diversity within a honeybee colony increases the variation in the frequency of tasks performed by workers. We show that genotypically diverse colonies, each composed of 20 subfamilies, collect more pollen than do genotypically similar colonies, each composed of a single subfamily. However, genotypically similar colonies collect greater varieties of pollen than do genotypically diverse colonies. Further, the composition of collected pollen types is less similar among genotypically similar colonies than among genotypically diverse colonies. The response threshold model predicts that genotypic subsets of workers vary in their response to task stimuli. Consistent with this model, our findings suggest that genotypically diverse colonies likely send out fewer numbers of foragers that independently search for pollen sources (scouts) in response to protein demand by the colony, resulting in a lower variety of collected pollen types. The cooperative foraging strategy of honeybees involves a limited number of scouts monitoring the environment that then guide the majority of foragers to high quality food sources. The genetic composition of the colony appears to play an important role in the efficiency of this behavior.     

Directional change in a suite of foraging behaviors in tropical and temperate evolved honey bees (<Emphasis Type="Italic">Apis mellifera</Emphasis> L.)

The concept of a suite of foraging behaviors was introduced as a set of traits showing associative directional change as a characterization of adaptive evolution. I report how naturally selected differential sucrose response thresholds directionally affected a suite of honey bee foraging behaviors. Africanized and European honey bees were tested for their proboscis extension response thresholds to ascending sucrose concentrations, reared in common European colonies and, captured returning from their earliest observed foraging flight. Race constrained sucrose response threshold such that Africanized bees had significantly lower sucrose response thresholds. A Cox proportional hazards regression model of honey bee race and sucrose response threshold indicated that Africanized bees were 29% (P<0.01) more at risk to forage over the 30-day experimental period. Sucrose response threshold organized age of first foraging such that each unit decrease in sucrose response threshold increased risk to forage by 14.3% (P<0.0001). Africanized bees were more likely to return as pollen and water foragers than European foragers. Africanized foragers returned with nectar that was significantly less concentrated than European foragers. A comparative analysis of artificial and naturally selected populations with differential sucrose response thresholds and the common suite of directional change in foraging behaviors is discussed. A suite of foraging behaviors changed with a change in sucrose response threshold that appeared as a product of functional ecological adaptation.Communicated by R.F.A. Moritz     

The early bee catches the flower - circadian rhythmicity influences learning performance in honey bees, <Emphasis Type="Italic">Apis mellifera</Emphasis>

Circadian rhythmicity plays an important role for many aspects of honey bees’ lives. However, the question whether it also affects learning and memory remained unanswered. To address this question, we studied the effect of circadian timing on olfactory learning and memory in honey bees Apis mellifera using the olfactory conditioning of the proboscis extension reflex paradigm. Bees were differentially conditioned to odours and tested for their odour learning at four different “Zeitgeber” time points. We show that learning behaviour is influenced by circadian timing. Honey bees perform best in the morning compared to the other times of day. Additionally, we found influences of the light condition bees were trained at on the olfactory learning. This circadian-mediated learning is independent from feeding times bees were entrained to, indicating an inherited and not acquired mechanism. We hypothesise that a co-evolutionary mechanism between the honey bee as a pollinator and plants might be the driving force for the evolution of the time-dependent learning abilities of bees.     

Reversible royalty in worker honeybees (<Emphasis Type="Italic">Apis mellifera</Emphasis>) under the queen influence

In most social insects, worker sterility is reversible, and in the absence of the queen, at least some workers develop ovaries and lay male-destined eggs. In the honeybee, reproductive workers also produce queen-characteristic mandibular and Dufour’s pheromones. The evolution of worker sterility is still under debate as to whether it is caused by queen manipulation (queen-control hypothesis) or represents worker fitness maximization (worker-control hypothesis). In this study, we investigated whether worker fertility and royal pheromone production are reversible under the queen influence. To that effect, we induced ovary activation and queen pheromone production in workers by rearing them as queenless (QL) groups. These workers were subsequently reintroduced into queenright (QR) microcolonies for 1 week, and their ovary status and queen pheromone levels were monitored. Workers reintroduced into QR, but not QL colonies, showed a clear regression in ovary development and levels of the queen pheromones. This is the first demonstration that worker sterility and/or fertility is reversible and is influenced by the queen. These results also emphasize the robustness of the coupling between ovary activation and royal pheromone production, as well as lending credence to the queen-control hypothesis. The dynamics of queen pheromone production in QL workers supports the role of Dufour’s gland pheromone as a fertility signal and that of the mandibular gland pheromone in dominance hierarchies.The two authors, Osnat Malka and Shiri Shnieor, contributed equally to this work.     

Sperm utilization pattern in the honeybee (<Emphasis Type="Italic">Apis mellifera</Emphasis>)

Queen honeybees (Apis mellifera) mate with a large number of drones on their nuptial flights. Not all drones contribute equally to the queens offspring and the queens utilization pattern of spermatozoa from different drones has an important impact on the genetic composition of the colony. Here we study the consequences of sperm use for the fitness of the queens mates with microsatellite DNA-fingerprinting. Eight queens were instrumentally inseminated with semen of six or seven drones. Each drone contributed either 0.5 µl or 1.0 µl semen, respectively, and we analyzed both the impact of the insemination sequence and the amount of semen on the sperm utilization. Our data show no significant effect of the insemination sequence but a strong impact of the semen volume of a drone on the frequency of his worker offspring in the colony. This effect was not linear and the patriline frequencies of the drones contributing larger semen volumes are disproportionately enhanced. If these observations are also valid for natural matings, drone honeybees should maximize the number of sperm but not apply specific mating tactics to be first or last male in a mating sequence.Communicated by R. PageAn erratum to this article can be found at     

The effect of foraging specialization on various learning tasks in the honey bee (<Emphasis Type="Italic">Apis mellifera</Emphasis>)

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.     

Nestmate recognition for eggs in the honeybee (<Emphasis Type="Italic">Apis mellifera</Emphasis> L.)

Colony integrity is fundamental to social insects and is threatened by the reproduction of non-nestmates. Therefore, discrimination between eggs derived from nestmates and non-nestmates would constitute an adaptation to prevent exploitation of the entire cooperative group by unrelated individuals. The removal of nestmate and non-nestmate queen and worker-laid eggs was evaluated in honeybees using colonies of Apis mellifera capensis to test female and of A. m. scutellata to test male eggs. The data show that honeybees can distinguish between nestmate and non-nestmate eggs of both sexes. Moreover, non-nestmate female queen-laid eggs were removed significantly faster than nestmate female worker-laid eggs in A. m. capensis, indicating that nestmate recognition cues can override caste-specific ones. While the experimental manipulation accounts for 37.2% (A. m. scutellata) or 1.6% (A. m. capensis) of variance in relation to egg removal, nestmate recognition explains 33.3% for male eggs (A. m. scutellata) and 60.6% for female eggs (A. m. capensis), which is almost twice as high as the impact of caste (16.7% A. m. scutellata; 25% A. m. capensis). Our data show a stronger effect of nestmate recognition on egg removal in the honeybee, suggesting that cues other than caste-specific ones (viability/kin) can dominate egg removal behavior. In light of intraspecific social parasitism, preventing the reproduction of unrelated individuals (group selection) rather than preferring queens’ eggs (kin selection) appears to be the driving force behind the evolution of egg removal behavior in honeybees.     

Effects of protein-constrained brood food on honey bee (<Emphasis Type="Italic">Apis mellifera</Emphasis> L.) pollen foraging and colony growth

Pollen is the sole source of protein for honey bees, most importantly used to rear young. Honey bees are adept at regulating pollen stores in the colonies based on the needs of the colony. Mechanisms for regulation of pollen foraging in honey bee are complex and remain controversial. In this study, we used a novel approach to test the two competing hypothesis of pollen foraging regulation. We manipulated nurse bee biosynthesis of brood food using a protease inhibitor that interferes with midgut protein digestion, significantly decreasing the amount of protein extractable from hypopharyngeal glands. Experimental colonies were given equal amounts of protease inhibitor-treated and untreated pollen. Colonies receiving protease inhibitor treatment had significantly lower hypopharyngeal gland protein content than controls. There was no significant difference in the ratio of pollen to nonpollen foragers between the treatments. Pollen load weights were also not significantly different between treatments. Our results supported the pollen foraging effort predictions generated from the direct independent effects of pollen on the regulation of pollen foraging and did not support the prediction that nurse bees regulate pollen foraging through amount of hypopharyngeal gland protein biosynthesis.     

Degree-day accumulation controlling allopatric and sympatric variations in the sociality of sweat bees, <Emphasis Type=Italic>Lasioglossum</Emphasis> (<Emphasis Type=Italic>Evylaeus</Emphasis>) <Emphasis Type=Italic>baleicum</Emphasis> (Hymenoptera: Halictidae)

Halictine bees exhibit a wide range of social behaviour that varies both inter- and intraspecifically. Although previous studies suggested that the intraspecific variation might be attributed to temperature differences, there was no direct evidence to detect the relationships between temperature and socialities. Lasioglossum (Evylaeus) baleicum exhibited solitary behaviour in a cooler locality (Kawakita) because of the shorter breeding season; in a warmer locality (Nishioka Park), however, this bee species exhibited eusociality at sunny site and solitary behaviour at shady site, whereas a molecular phylogeny confirms that all of these colonies are evidently conspecific. Therefore, we examined the effect of degree-day accumulation on the sympatric social variation of L. baleicum by rearing the bees to calculate the threshold temperature. Whereas they showed high mortality, the threshold temperature was estimated to be 10.33°C and the expected degree-day accumulation was 340 degree days. When we use this value of a degree-day accumulation to estimate the expected eclosion date, the estimated dates were always consistent with observed eclosion dates. In any sites where the bees were solitary, the degree-day accumulation was not enough for the second eclosion by the end of the bee-active season. In Nishioka Park, sex ratio of the first brood was female biased, and daughters were smaller than mothers; in Kawakita, however, there was no sex bias, and daughters were as large as their mothers indicating that the foundresses seem to produce gyne-sized females in Kawakita but worker-sized females in Nishioka though these females do not become workers at shady site.     

Monitoring acoustically tagged king prawns <Emphasis Type=Italic>Penaeus</Emphasis> (<Emphasis Type=Italic>Melicertus</Emphasis>) <Emphasis Type=Italic>plebejus</Emphasis> in an estuarine lagoon

Fine-scale movement patterns in penaeid prawns are rarely observed in situ, but are essential in understanding habitat use, foraging, and anti-predator behaviour. Acoustic telemetry was applied to examine the activity, space utilization, and habitat use of the eastern king prawn Penaeus (Melicertus) plebejus, at small temporal and spatial scales. Tracking of sub-adult P. plebejus (n = 9) in Wallagoot Lake (36.789°S, 149.959°E; 23 April–12 May 2009) and calculation of a minimum activity index (MAI) revealed high variation in activity rates across diel periods and in different habitats. Elevated activity rates and movement indicated foraging in unvegetated habitats during the night. Areas within the 95 and 50% space utilization contours averaged 2,654.1 ± 502.0 and 379.9 ± 103.9 m², respectively, and there was a significant negative relationship between these areas and prawn activity rates in unvegetated habitats. This study provides the first estimates of prawn activity rates and space utilization in the field. Application of acoustic telemetry can increase knowledge of prawn movements and their interactions with other marine species in different habitats.     

The effect of repeated vibration signals on worker behavior in established and newly founded colonies of the honey bee, <Emphasis Type="Italic">Apis mellifera</Emphasis>

Communication signals used in animal social interactions are frequently performed repetitively, but the function of this repetition is often not well understood. We examined the effects of signal repetition by investigating the behavior of worker honey bees that received differing numbers of vibration signals in established and newly founded colonies, which could use signal repetition differently to help adjust task allocations to the labor demands associated with the different stages of colony development. In both colony types, more than half of all monitored workers received more than one vibration signal, and approximately 12% received ≥5 signals during a given 20-min observation period. Vibrated recipients exhibited greater activity and task performance than same-age non-vibrated controls at all levels of signal activity. However, vibrated workers showed similar levels of task performance, movement rates, cell inspection rates, and trophallactic exchanges regardless of the number of signals received. Thus, the repeated performance of vibration signals on individual bees did not cause cumulative increases in the activity of certain workers, but rather may have functioned to maintain relatively constant levels of activity and task performance among groups of recipients. The established and newly founded colonies did not differ in the extent to which individual workers received the different numbers of vibration signals or in the levels of activity stimulated by repeated signals. Previous work has suggested that compared to established colonies, newly founded colonies have a greater number of vibrators that perform signals on a greater proportion of the workers they contact. Taken in concert, these results suggest that vibration signal repetition may help to adjust task allocations to the different stages of colony development by helping to maintain similar levels of activity among a greater total number of recipients, rather than by eliciting cumulative effects that cause certain recipients to work harder than others.     

Behavioral adaptations of the cubozoan medusa <Emphasis Type="Italic">Tripedalia cystophora</Emphasis> for feeding on copepod (<Emphasis Type="Italic">Dioithona oculata</Emphasis>) swarms

The cubozoan medusa Tripedalia cystophora preys on dense swarms of the copepod Dioithona oculata in the mangrove prop-root habitat of Puerto Rico. The copepod swarms form in shafts of sunlight that penetrate the mangrove canopy during the day. T. cystophora are found primarily within the same illuminated areas, feeding heavily on the dense swarms of copepods. Laboratory studies were conducted to examine the behavioral adaptations of T. cystophora that allow them to remain within these dense copepod swarms. In the presence of vertical light shafts, T. cystophora showed both a significant change in swimming speed and a significant increase in turning rate. T. cystophora turn abruptly when they leave a vertical shaft of light and quickly re-enter. The presence or absence of copepod prey, either in swarms or dispersed, had no significant effect on T. cystophora swimming speed or turning behavior. Feeding rates of T. cystophora on the copepod D. oculata increase rapidly with copepod density, and maximum rates are not achieved until the high densities associated with swarms are reached. It seems doubtful that these small medusae could survive without their ability to encounter and exploit these dense swarms of copepods.     

Levels of selection in a social insect: a review of conflict and cooperation during honey bee (<Emphasis Type="Italic">Apis mellifera</Emphasis>) queen replacement

The extended phenotype of a social insect colony enables selection to act at both the individual level (within-colony selection) and the colony level (between-colony selection). Whether a particular trait persists over time depends on the relative within- and between-colony selection pressures. Queen replacement in honey bee colonies exemplifies how selection may act at these different levels in opposing directions. Normally, a honey bee colony has only one queen, but a colony rears many new queens during the process of colony reproduction. The replacement of the mother queen has two distinct phases: queen rearing, where many queens develop and emerge from their cells, and queen elimination, where most queens die in a series of fatal duels. Which queens are reared to adulthood and which queens ultimately survive the elimination process depends on the strength and direction of selection at both the individual and colony levels. If within-colony selection is predominant, then conflict is expected to occur among nestmates over which queens are produced. If between-colony selection is predominant, then cooperation is expected among nestmates. We review the current evidence for conflict and cooperation during queen replacement in honey bees during both the queen rearing and queen elimination phases. In particular, we examine whether workers of different subfamilies exhibit conflict by acting nepotistically toward queens before and after they have emerged from their cells, and whether workers exhibit cooperation by collectively producing queens of high reproductive quality. We conclude that although workers may weakly compete through nepotism during queen rearing, workers largely cooperate to raise queens of similar reproductive potential so that any queen is suitable to inherit the nest. Thus it appears that potential conflict over queen replacement in honey bees has not translated into actual conflict, suggesting that between-colony selection predominates during these important events in a colonys life cycle.Communicated by A. Cockburn     

Differential reproductive success among subfamilies in queenless honeybee (<Emphasis Type="Italic">Apis mellifera</Emphasis> L.) colonies

With very rare exceptions, queenright worker honeybees (Apis mellifera L.) forego personal reproduction and suppress reproduction by other workers, preferring to rear the queens sons. This is in stark contrast to colonies that have lost their queen and have failed to rear a replacement. Under these conditions workers activate their ovaries and lay many eggs that develop parthenogenetically into a final brood of males (drones) before the colony perishes. Interestingly, not all workers contribute equally to this final generation of drones in queenless colonies. Some subfamilies (workers that share the same father) contribute a disproportionately greater number of offspring than other subfamilies. Here we explore some of the mechanisms behind this reproductive competition among subfamilies. We determined the relative contribution of different subfamilies present in colonies to laying workers, eggs, larvae and pupae by genotyping samples of all life stages using a total of eight microsatellite loci. Our colonies were headed by free-mated queens and comprised 8–17 subfamilies and therefore differed significantly from colonies used in an earlier study investigating the same phenomena where colonies comprised an artificially low number of subfamilies. We show that, first, subfamilies vary in the speed with which they activate their ovaries after queen-loss and, second, that the survival of eggs to the larval stage is unequal among subfamilies suggesting that some subfamilies lay eggs that are more acceptable than others. However, there is no statistically significant difference among subfamilies in the survival of larvae to pupae, indicating that ovary activation and egg survival are the critical components to reproductive competition among subfamilies of queenless honeybee workers.Communicated by R. Page     

Aging and demographic plasticity in response to experimental age structures in honeybees (<Emphasis Type="Italic">Apis mellifera</Emphasis> L)

Honeybee colonies are highly integrated functional units characterized by a pronounced division of labor. Division of labor among workers is mainly age-based, with younger individuals focusing on in-hive tasks and older workers performing the more hazardous foraging activities. Thus, experimental disruption of the age composition of the worker hive population is expected to have profound consequences for colony function. Adaptive demography theory predicts that the natural hive age composition represents a colony-level adaptation and thus results in optimal hive performance. Alternatively, the hive age composition may be an epiphenomenon, resulting from individual life history optimization. We addressed these predictions by comparing individual worker longevity and brood production in hives that were composed of a single-age cohort, two distinct age cohorts, and hives that had a continuous, natural age distribution. Four experimental replicates showed that colonies with a natural age composition did not consistently have a higher life expectancy and/or brood production than the single-cohort or double-cohort hives. Instead, a complex interplay of age structure, environmental conditions, colony size, brood production, and individual mortality emerged. A general tradeoff between worker life expectancy and colony productivity was apparent, and the transition from in-hive tasks to foraging was the most significant predictor of worker lifespan irrespective of the colony age structure. We conclude that the natural age structure of honeybee hives is not a colony-level adaptation. Furthermore, our results show that honeybees exhibit pronounced demographic plasticity in addition to behavioral plasticity to react to demographic disturbances of their societies.