Nest site selection in the open-nesting honeybee Apis florea

We studied nest site selection by swarms of the red dwarf honeybee, Apis florea. By video recording and decoding all dances of four swarms, we were able to determine the direction and distances indicated by 1,239 dances performed by the bees. The bees also performed a total of 715 nondirectional dances; dances that were so brief that no directional information could be extracted. Even though dances converged over time to a smaller number of areas, in none of the swarms did dances converge to one site. As a result, even prior to lift off, bees performed dances indicating nest sites in several different directions. Two of four swarms traveled directly in what seemed to be the general direction indicated by the majority of dances in the half hour prior to swarm lift off. The other two traveled along circuitous routes in the general direction indicated by the dances. We suggest that nest site selection in A. florea has similar elements to nest site selection in the better-studied Apis mellifera. However, the observation that many more locations are indicated by dances prior to lift off also shows that there are fundamental differences between the two species.     

Quorum sensing during nest-site selection by honeybee swarms

This study addresses a question about the nest-site selection process of honeybee swarms: how do the scout bees know when to initiate the preparation for their swarm’s move to their new home? We tested the quorum-sensing hypothesis: that the scouts do this by noting when one of the potential nest sites under consideration is being visited by a sufficiently large number of scouts. A falsifiable prediction of this hypothesis is that delaying the formation of a quorum of scout bees at a swarm’s chosen nest cavity, while leaving the rest of the decision-making process undisturbed, should delay the start of worker piping (the prepare-for-takeoff signal) and thus the takeoff of the swarm. In paired trials, we presented each of four swarms once with five nest boxes close to each other at a site and once with a single nest box. The multiple nest boxes caused the scouts visiting the site to be dispersed among five identical nest cavities rather than concentrated at one. We observed long delays in the start of piping and the start of takeoff in the five-nest-box trials relative to the one-nest-box trials. These results provide strong support for the quorum-sensing hypothesis.     

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     

Coordinating a group departure: who produces the piping signals on honeybee swarms?

A swarm of honeybees provides a striking example of an animal group performing a synchronized departure for a new location; in this case, thousands of bees taking off at once to fly to a new home. However, the means by which this is achieved remain unclear. Shortly before takeoff, one hears a crescendo of a high-pitched mechanical signal—worker piping—so we explored the role of this signal in coordinating a swarm’s mass takeoff. Specifically, we examined whether exclusively nest site scouts produce the worker piping signal or whether it is produced in a relay or chain reaction fashion. We found no evidence that bees other than the scouts that have visited the swarm’s chosen nest site produce piping signals. This absence of relay communication in piping suggests that it is a signal that only primes swarms for takeoff and that the release of takeoff is triggered by some other signal or cue; perhaps the takeoff of bees on the swarm periphery as they reach flight temperature in response to piping.     

Acoustical signals in the dance language of the giant honeybee,Apis dorsata

Summary Acoustical signals emitted by dancing bees have recently been shown to transmit information about the location of food sources in the western honeybee, Apis mellifera. Towne (1985) reported that in the Asian honeybee species Apis dorsata, which builds a single comb in the open under overhanging rocks or tree branches, sound signals were not emitted by the dancers. This led to the conclusion that acoustical communication is restricted to bees that nest in the dark, like A. mellifera. Here we show that in fact A. dorsata produces dance sounds similar to those emitted by A. mellifera, and that these acoustical signals contain information about distance, direction and profitability of food sources. The acoustical transfer of information has thus evolved independently of nesting in dark cavities. The significance of nocturnal activity in Apis dorsata for the evolution of sound communication is discussed. Correspondence to: W.H. Kirchner     

Dance precision of <Emphasis Type="Italic">Apis florea</Emphasis>—clues to the evolution of the honeybee dance language?

All honeybee species make use of the waggle dance to communicate the direction and distance to both food sources and potential new nest sites. When foraging, all species face an identical problem: conveying information about profitable floral patches. However, profound differences in nesting biology (some nest in cavities while others nest in the open, often on a branch or a cliff face) may mean that species have different requirements when dancing to advertise new nest sites. In cavity nesting species, nest sites are a precise location in the landscape: usually a small opening leading to a cavity in a hollow tree. Dances for cavities therefore need to be as precise as possible. In contrast, when the potential nest site comprises a tree or perhaps seven a patch of trees, precision is less necessary. Similarly, when a food patch is advertised, dances need not be very precise, as floral patches are often large, unless they are so far away that recruits need more precise information to be able to locate them. In this paper, we study the dance precision of the open-nesting red dwarf bee Apis florea. By comparing the precision of dances for food sources and nest sites, we show that A. florea workers dance with the same imprecision irrespective of context. This is in sharp contrast with the cavity-nesting Apis mellifera that increases the precision of its dance when advertising a potential new home. We suggest that our results are in accordance with the hypothesis that the honeybees’ dance communication initially evolved to convey information about new nest sites and was only later adapted for the context of foraging.     

Choosing a home: how the scouts in a honey bee swarm perceive the completion of their group decision making

This study considers the mystery of how the scout bees in a honey bee swarm know when they have completed their group decision making regarding the swarm's new nest site. More specifically, we investigated how the scouts sense when it is appropriate for them to begin producing the worker piping signals that stimulate their swarm-mates to prepare for the flight to their new home. We tested two hypotheses: "consensus sensing," the scouts noting when all the bees performing waggle dances are advertising just one site; and "quorum sensing," the scouts noting when one site is being visited by a sufficiently large number of scouts. Our test involved monitoring four swarms as they discovered, recruited to, and chose between two nest boxes and their scouts started producing piping signals. We found that a consensus among the dancers was neither necessary nor sufficient for the start of worker piping, which indicates that the consensus sensing hypothesis is false. We also found that a buildup of 10–15 or more bees at one of the nest boxes was consistently associated with the start of worker piping, which indicates that the quorum sensing hypothesis may be true. In considering why the scout bees rely on reaching a quorum rather than a consensus as their cue of when to start preparing for liftoff, we suggest that quorum sensing may provide a better balance between accuracy and speed in decision making. In short, the bees appear to begin preparations for liftoff as soon as enough of the scout bees, but not all of them, have approved of one of the potential nest sites.

An oligarchy of nest-site scouts triggers a honeybee swarm’s departure from the hive

Animals that travel in groups must synchronize the timing of their departures to assure cohesion of the group. While most activities in large colonies of social insects have decentralized control, certain activities (e.g., colony migration) can have centralized control, with only a special subset of well-informed individuals making a decision that affects the entire colony. We recently discovered that a small minority of individuals in a honeybee colony—an oligarchy—decides when to trigger the departure of a swarm from its hive. The departure process begins with some bees producing the worker-piping signal (the primer for departure) and is followed by these bees producing the buzz-run signal (the releaser for departure). In this study, we determined the identity of these signalers. We found that a swarm’s nest-site scouts search for potential nest cavities prior to the departure of the swarm from its hive. Furthermore, we found that the predeparture nest-site scouts are the sole producers of the worker-piping signal and that they are the first producers of the buzz-run signal. The control of the departure of a honeybee swarm from its hive shows how a small minority of well-informed individuals in a large social insect colony can make important decisions about when a colony should take action.     

Consistent personality differences in house-hunting behavior but not decision speed in swarms of honey bees (<Emphasis Type="BoldItalic">Apis mellifera</Emphasis>)

Speed-accuracy tradeoffs are a common feature of decision-making processes, both in individual animals and in groups of animals working together to reach a single collective decision. Individual organisms display consistent differences in their “impulsivity,” and vary in their tendency to make rapid, impulsive choices as opposed to slower, more accurate decisions. However, we do not yet know whether groups of animals consistently differ in their tendency to prioritize decision speed over accuracy. We challenged 17 swarms of honey bees (Apis mellifera) to simultaneously choose a new nest site in each of three locations, and measured their decision speeds in each trial. We found that swarms displayed consistent personality differences in the number of waggle dances and shaking signals they performed and in how actively they scouted for new nest sites. However, swarms did not consistently differ in how long they took to choose a nest site. We suggest that house-hunting A. mellifera swarms may place an especially high emphasis on decision accuracy when choosing a nest site, and that chance events—such as the time when each swarm discovers a sufficiently high-quality nest site—may consequently play a greater role in determining a swarm’s decision speed than intrinsic characteristics such as a swarm’s “impulsivity.”     

Levels of polyandry and intracolonial genetic relationships in Apis florea

DNA was extracted from worker and drone pupae of each of five colonies of the dwarf honey bee Apis florea. Polymerase chain reactions (PCR) were conducted on DNA extracts using five sets of primers known to amplify microsatellite loci in A. mellifera. Based on microsatellite allele distributions, queens of the five colonies mated with at least 5–14 drones. This is up to 3 times previous maximum estimates obtained from sperm counts. The discrepancy between sperm count and microsatellite estimates of the number of matings in A. florea suggests that despite direct injection of semen into the spermatheacal duct, either A. florea drones inject only a small proportion of their semen, or queens are able to rapidly expel excess semen after mating. A model of sexual selection (first proposed by Koeniger and Koeniger) is discussed in which males attempt to gain reproductive dominance by increasing ejaculate volume and direct injection of spermatozoa into the spermatheca, while queens attempt to maintain polyandry by retaining only a small fraction of each male's ejaculate. It is shown, at least in this limited sample, that the effective number of matings is lower in A. florea than in A. mellifera.     

Preservation and loss of the honey bee (<Emphasis Type="Italic">Apis</Emphasis>) egg-marking signal across evolutionary time

Honey bee workers are able to distinguish queen-laid eggs from worker-laid eggs, and remove (‘police’) worker-laid eggs. The cue that police workers use is as yet unidentified but is likely to be a chemical signal. This signal benefits queens for it ensures their reproductive monopoly. It also benefits collective workers because it allows them to raise more closely related queen-laid males than the less-related sons of half sisters. Because both parties benefit from the egg-marking signal, it should be stable over evolutionary time. We show that Apis mellifera workers can distinguish queen-laid from worker-laid eggs of the dwarf honey bee A. florea, a phylogenetically distant species that diverged from the A. mellifera lineage 6–10 mya. However, A. mellifera workers are unable to distinguish worker-laid eggs of A. cerana, a much more recent divergence (2–3 mya). The apparent change in the egg-marking signal used by A. cerana may be associated with the high rates of ovary activation in this species.     

The reproductive dilemmas of queenless red dwarf honeybee (Apis florea) workers

Honeybee (Apis) workers cannot mate, but retain functional ovaries. When colonies have lost their queen, many young workers begin to activate their ovaries and lay eggs. Some of these eggs are reared, but most are not and are presumably eaten by other workers (worker policing). Here we explore some of the factors affecting the reproductive success of queenless workers of the red dwarf honeybee Apis florea. Over a 2-year period we collected 40 wild colonies and removed their queens. Only two colonies remained at their translocated site long enough to rear males to pupation while all the others absconded. Absconding usually occurred after worker policing had ceased, as evidenced by the appearance of larvae. Dissections of workers from eight colonies showed that in A. florea, 6% of workers have activated ovaries after 4 days of queenlessness, and that 33% of workers have activated ovaries after 3 weeks. Worker-laid eggs may appear in nests within 4 days and larvae soon after, but this is highly variable. As with Apis mellifera, we found evidence of unequal reproductive success among queenless workers of A. florea. In the two colonies that reared males to pupation and which we studied with microsatellites, some subfamilies had much higher proportions of workers with activated ovaries than others. The significance of absconding and internest reproductive parasitism to the alternative reproductive strategies of queenless A. florea workers is discussed.     

Nest-Site Selection in Individual Loggerhead Turtles and Consequences for Doomed-Egg Relocation

Abstract:  Relocation of eggs is a common strategy for conservation of declining reptilian populations around the world. If individuals exhibit consistency in their nest-site selection and if nest-site selection is a heritable trait, relocating eggs deposited in vulnerable locations may impose artificial selection that would maintain traits favoring unsuccessful nest-site selection. Conversely, if most individuals scatter their nesting effort and individuals that consistently select unsuccessful nest sites are uncommon, then artificial selection would be less of a concern. During the 2005 nesting season of loggerhead turtles ( Caretta caretta ) at Mon Repos beach, Queensland, Australia, we measured the perpendicular distance from the original nest site to a stationary dune baseline for in situ (unrelocated) and relocated clutches of eggs. We observed the fate of in situ clutches and predicted what would have been the fate of relocated clutches if they had not been moved by mapping tidal inundation and storm erosion lines. In 2005 turtles deposited an average of 3.84 nests and did not consistently select nest sites at particular distances from the stationary dune baseline. Selection of unsuccessful nest sites was distributed across the nesting population; 80.3% of the turtles selected at least one unsuccessful nest site and when previous breeding seasons were included, 97% selected at least one unsuccessful nest site. Females with nesting experience selected more successful nest sites than females with little or no experience. Relocating eggs vulnerable to tidal inundation and erosion saves the progeny from a large percentage of the population and the progeny from individuals who may in subsequent years nest successfully. Our results suggest that doomed-egg relocation does not substantially distort the gene pool in the eastern Australian loggerhead stock and should not be abandoned as a strategy for the conservation of marine turtle populations.     

Lack of interspecific parasitism between the dwarf honeybees Apis andreniformis and Apis florea

The dwarf honeybees Apis florea and Apis andreniformis are sympatric in Southeast Asia. We examined undisturbed nests of both species finding that heterospecific workers are present in some nests at low frequency. This suggested that workers may enter heterospecific nests as a prelude to reproductive parasitism. To test this hypothesis, we created mixed-species colonies and determined the reproductive response of workers within them based on molecular markers. In queenless colonies, workers of both species activated their ovaries at equal frequency. However, the majority species, A. florea, had complete reproductive dominance over A. andreniformis, most likely because the A. florea workers recognised and removed heterospecific larvae. In queenright mixed-species colonies, workers responded to heterospecific signals of the presence of the queen and did not activate their ovaries. Thus, despite predictions from kin selection theory that workers would benefit from parasitising heterospecific nests, we find no evidence that selection has established a parasitic strategy in these sibling species.     

Genotypic variability in age polyethism and task specialization in the honey bee,Apis mellifera (Hymenoptera: Apidae)

Summary The currently accepted model for division of labor in honey bees, Apis mellifera, explains variation in the frequency at which workers perform specific tasks as the result of differences in age and environment. Although well documented, the model is incomplete because it fails to take genotypic variability among workers into account. We show that workers from two genetically distinct strains of honey bees differed in the age at which they began foraging and in the relative frequency at which they foraged for pollen. Workers from the two strains also exhibited significant spatial heterogeneity within the nest, suggesting that they differed in the frequency at which they performed within-nest tasks as well. A heuristic model of division of labor that incorporates genotypic effects is presented.     

Variation in nesting patterns affecting nest temperatures in two populations of painted turtles (<Emphasis Type="Italic">Chrysemys picta</Emphasis>) with temperature-dependent sex determination

Mechanisms maintaining sex ratios in populations with temperature-dependent sex determination (TSD) remain elusive. Although geographic variation in embryonic sex determination (i.e., pivotal temperature) has been widely investigated in reptiles exhibiting TSD, no previous studies have directly addressed geographic variation in maternal behavior affecting nest thermal conditions. I evaluated patterns of nest-site selection and its effects on thermal and hydric nest conditions for a population of painted turtles ( Chrysemys picta bellii) exhibiting TSD in New Mexico. These results are compared to data collected from a well-studied, conspecific population experiencing relatively cooler climatic conditions in Illinois. Since canopy vegetation cover reduces nest temperatures in Illinois, I expected females in New Mexico to nest under high amounts of canopy vegetation cover. However, females from New Mexico placed nests under significantly less canopy vegetation cover, but closer to standing water, than did females from Illinois. Experimental nests in New Mexico demonstrated that increased canopy vegetation cover and soil moisture reduced nest temperatures. By nesting close to standing water rather than under canopy vegetation cover, females in New Mexico nested in habitats more closely associated with maximizing moisture around nests rather than reducing nest temperatures through shading. Mean July nest temperatures were similar for both populations. Since nest hydric conditions affect hatching success and hatchling size in C. picta, nesting patterns in New Mexico may primarily reflect selection for microhabitats affecting offspring survivorship or size.     

Acoustic and visual cues in the dances of four honey bee species

Summary The sounds produced during the dance of the European honey bee, Apis mellifera, are potentially important in the reception of the dance information by recruit bees. I have studied the dances of the three Asian honey bee species and have found that the single species which nests in dark cavities like A. mellifera produces similar sounds, while the two open-nesting species produce none. This and other evidence suggest that the different species may perceive their dances through different sensory channels.     

Consensus building during nest-site selection in honey bee swarms: the expiration of dissent

This study addresses a question that lies at the heart of understanding how the scouts in a honey bee swarm achieve unanimity in their dances, and so reach agreement in their choice of a future nest site: what causes the scouts that perform dances for the non-chosen sites to stop dancing for these sites? One possibility is that a scout stops dancing for a non-chosen site only after she follows a lively dance for another site, such as the site that is ultimately chosen. This hypothesis is contradicted by the finding that 23 out of 27 scouts (in 6 swarms) that danced initially for a non-chosen site stopped their dancing before they followed a dance for another site. Evidently, a scout that supports initially one of the non-chosen sites is likely to withdraw her support for this site even before she learns about another site. What causes her to do so? Close examination of the behavior of scouts revealed that they reduce the strength of their dancing (waggle runs/return to the swarm) for a given site over consecutive returns to the swarm. On average, the pattern of this reduction in dancing is strikingly linear, which suggests that it arises from an internal, neurophysiological process that automatically drives down a scout's motivation to dance for a site. Other results suggest that scouts from inferior sites start their dancing less strongly, and so cease their dancing more rapidly, than do scouts from superior sites. If so, then during the consensus-building process of the scouts, it is the support (the dancing) for inferior sites that is most likely to die out while it is the support for a superior site that is most likely to prevail.     

Task specialization in a wild bee,Apis florea (Hymenoptera: Apidae), revealed by RFLP banding

Workers in a wild in situ colony of the dwarf honey bee, Apis florea, were observed undertaking the following behavior: liquid foraging, pollen foraging, guarding, stinging, fanning and wagging abdomen. Bees of each behavioral class were separately collected and frozen. Collections were made over a period of 10 days. Random samples of brood and workers were also collected. DNA was extracted from each bee and fingerprinted using a probe of unknown sequence obtained from an A. mellifera genomic library. Patterns of fingerprints (Fig. 1) were dissimilar among behavioral classes (Tables 1 and 2), strongly suggesting a genetic component to division of labor in this species. This result supports similar findings in A. mellifera in a species that is not troubled by many of the experimental difficulties inherent in A. mellifera. Correspondence to: B.P. Oldroyd