Worker policing and worker reproduction in Apis cerana

Workers of the Asian hive bee, Apis cerana, are shown to have relatively high rates of worker ovary activation. In colonies with an active queen and brood nest, 1-5% of workers have eggs in their ovarioles. When A. cerana colonies are dequeened, workers rapidly activate their ovaries. After 4 days 15% have activated ovaries and after 6 days, 40%. A cerana police worker-laid eggs in the same way that A. florea and A. mellifera do, but are perhaps slightly more tolerant of worker-laid eggs than the other species. Nevertheless, no worker's sons were detected in a sample of 652 pupal males sampled from 4 queenright colonies. A cerana continue to police worker-laid eggs, even after worker oviposition has commenced in a queenless colony.     

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.     

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     

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.     

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.     

Worker allocation in insect societies: coordination of nectar foragers and nectar receivers in honey bee (Apis mellifera) colonies

Nectar collection in the honey-bee is partitioned. Foragers collect nectar and take it to the nest, where they transfer it to receiver bees who then store it in cells. Because nectar is a fluctuating and unpredictable resource, changes in worker allocation are required to balance the work capacities of foragers and receivers so that the resource is exploited efficiently. Honey bee colonies use a complex system of signals and other feedback mechanisms to coordinate the relative and total work capacities of the two groups of workers involved. We present a functional evaluation of each of the component mechanisms used by honey bees – waggle dance, tremble dance, stop signal, shaking signal and abandonment – and analyse how their interplay leads to group-level regulation. We contrast the actual regulatory system of the honey bee with theory. The tremble dance conforms to predicted best use of information, where the group in excess applies negative feedback to itself and positive feedback to the group in shortage, but this is not true of the waggle dance. Reasons for this and other discrepancies are discussed. We also suggest reasons why honey bees use a combination of recruitment plus abandonment and not switching between subtasks, which is another mechanism for balancing the work capacities of foragers and receivers. We propose that the waggle and tremble dances are the primary regulation mechanisms, and that the stop and shaking signals are secondary mechanisms, which fine-tune the system. Fine-tuning is needed because of the inherent unreliability of the cues, queueing delays, which foragers use to make recruitment decisions. Received: 15 December 1998 / Received in revised form: 6 March 1999 / Accepted: 12 March 1999     

Worker reproductive parasitism and drift in the western honeybee Apis mellifera

When a honeybee (Apis spp.) colony loses its queen and is unable to rear a new one, some of the workers activate their ovaries and produce eggs. When a colony has a queen (i.e., it is queenright) almost all worker-laid eggs are eaten, but when hopelessly queenless, the workers become more tolerant of worker-laid eggs and rear some of them to adult drones. This increased tolerance renders a queenless colony vulnerable to worker reproductive parasitism, wherein unrelated workers enter the colony and lay eggs. Here, we show that the proportion of unrelated (non-natal) workers significantly decreases after an Apis mellifera colony becomes queenless. The remaining non-natal workers are as likely to have activated ovaries as natal workers, yet they produce more eggs than natal workers, resulting in significantly higher reproductive success for non-natal workers. In a second experiment, we provided queenless and queenright workers with a choice to remain in their own colony or to join a queenless or queenright colony nearby. The experiment was set up such that worker movement was unlikely to be due to simple orientation errors. Very few workers joined another colony, and there was no preference for workers to drift into or out of queenless or queenright colonies, in accordance with the proportion of non-natal workers declining significantly after becoming queenless in the first experiment.     

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.     

Kin structure and the swarming behavior of the honey bee Apis mellifera

Summary Experimental hives obtained from cordovan queens that were instrumentally inseminated with semen from one cordovan and one Italian drone were set up and allowed to swarm. Cordovan provides a resessive genetic marker system (cuticle color) so that the workers from the cordovan and Italian male lines are distinguishable. Our results show that these patrilineal worker groups segregate non-randomly during colony fission and this segregation cannot be explained by observed age structure. Evidence of innate kin recognition in bees has been previously established. We argue that kin recognition could be responsible for the observed non-random grouping of kin during swarming.     

Worker reproduction in honey-bees (Apis) and the anarchic syndrome: a review

Honey-bees, Apis, are an important model system for investigating the evolution and maintenance of worker sterility. The queen is the main reproductive in a colony. Workers cannot mate, but they can lay unfertilized eggs, which develop into males if reared. Worker reproduction, while common in queenless colonies, is rare in queenright colonies, despite the fact that workers are more related to their own sons than to those of the queen. Evidence that worker sterility is enforced by 'worker policing' is reviewed and worker policing is shown to be widespread in Apis. We then discuss a rare behavioural syndrome, 'anarchy', in which substantial worker production of males occurs in queenright colonies. The level of worker reproduction in these anarchic colonies is far greater than in a normal queenright honey-bee colony. Anarchy is a counterstrategy against worker policing and an example of a 'cheating' strategy invading a cooperative system.     

Maternity of replacement queens in the thelytokous Cape honey bee Apis mellifera capensis

Unlike workers of all other honey bee (Apis mellifera) subspecies, workers of the Cape honey bee of South Africa (A. mellifera capensis) reproduce thelytokously and are thus able to produce female offspring that are pseudoclones of themselves. This ability allows workers to compete with their queen over the maternity of daughter queens and, in one extreme case, has led to a clonal lineage of workers becoming a social parasite in commercially managed populations of A. mellifera scutellata. Previous work (Jordan et al., Proc R Soc Lond B Biol Sci 275:345, 2008) showed that, in A. mellifera capensis, 59% of queen cells produced during swarming events contained the offspring of workers and that, of these, 65% were the offspring of non-natal workers. Here, we confirm that a substantial proportion (38.5%) of offspring queens is worker-laid. We additionally show that: (1) Although queens produce most diploid female offspring sexually, we found some homozygous or hemizygous queen offspring, suggesting that queens also reproduce by thelytoky. These parthenogenetic individuals are probably nonviable beyond the larval stage. (2) Worker-laid offspring queens are viable and become the resident queen at the same frequency as do sexually produced queen-laid offspring queens. (3) In this study, all but one of the worker-derived queens were laid by natal workers rather than workers from another nest. This suggests that the very high rates of social parasitism observed in our previous study were enhanced by beekeeping manipulations, which increased movement of parasites between colonies.     

Reproductive competition in queenless honey bee colonies (Apis mellifera L.)

Previously we reported that there are subfamily differences in drone production in queenless honey bee colonies, but these biases are not always explained by subfamily differences in oviposition behavior. Here we determine whether these puzzling results are best explained by either inadequate sampling of the laying worker population or reproductive conflict among workers resulting in differential treatment of eggs and larvae. Using colonies composed of workers from electrophoretically distinct subfamilies, we collected samples of adult bees engaged in the following behavior: true egg laying, false egg laying, indeterminate egg laying, egg cannibalism, or nursing (contact with larvae). We also collected samples of drone brood at four different ages: 0 to 2.5-h-old eggs, 0 to 24-h-old eggs, 3 to 8-day-old larvae, and 9 to 14-day-old larvae and pupae. Allozyme analyses revealed significant subfamily differences in the likelihood of exhibiting egg laying, egg cannibalism, and nursing behavior, as well as significant subfamily differences in drone production. There were no subfamily differences among the different types of laying workers collected from each colony, suggesting that discrepancies between subfamily biases in egg-laying behavior and drone production are not due to inadequate sampling of the laying worker population. Subfamily biases in drone brood production within a colony changed significantly with brood age. Laying workers had significantly more developed ovaries than either egg cannibals or nurses, establishing a physiological correlate for the observed behavioral genetic differences. These results suggest there is reproductive conflict among subfamilies and individuals within queenless colonies of honey bees. The implications of these results for the evolution of reproductive conflict, in both queenright and queenless contexts, are discussed.     

Measurement of nest cavity volume by the honey bee (Apis mellifera)

Behavioral Ecology and Sociobiology -     

Preferences and tradeoffs in nectar temperature and nectar concentration in the Asian hive bee Apis cerana

Honey bee foragers need to asses and make trade-offs between a number of potentially conflicting floral attributes. Here, we investigate multi-attribute decision making in the eastern honey bee, Apis cerana, when foraging on food sources that varied in warmth and sucrose concentration. We show that foragers prefer warm (30 °C) sucrose solution over cool (10 °C) sucrose solution and concentrated (30 % w/w) sucrose solution over dilute (15 % w/w) sucrose solution. When we offered the preferred sucrose concentration (30 % w/w) at the less-preferred temperature (10 °C), and the less-preferred sucrose concentration (15 % w/w) at the preferred temperature (30 °C), foragers prioritized warmth by choosing the warmer, but lower concentration solution. When the temperature difference was less extreme, bees preferred more concentrated cooler syrup (30 % ww at 15 °C over 15 % 30 °C). However, the addition of a decoy item to the choice set had a significant effect on the bees' preferences. Our results highlight the critical importance of considering context effects when measuring the foraging preferences of animals.     

Heritable variation in learning performance affects foraging preferences in the honey bee (Apis mellifera)

There has now been an abundance of research conducted to explore genetic bases that underlie learning performance in the honey bee (Apis mellifera). This work has progressed to the point where studies now seek to relate genetic traits that underlie learning ability to learning in field-based foraging problems faced by workers. Accordingly, the focus of our research is to explore the correlation between laboratory-based performance using an established learning paradigm and field-based foraging behavior. To evaluate learning ability, selected lines were established by evaluating queens and drones in a proboscis extension reflex (PER) conditioning procedure to measure learning in a laboratory paradigm—latent inhibition (LI). Hybrid queens were then produced from our lines selected for high and low levels of LI and inseminated with semen from many drones chosen at random. The genetically diverse worker progeny were then evaluated for expression of LI and for preference of pollen and/or nectar during foraging. Foragers from several different queens, and which had resulted from fertilization by any of several different drone fathers, were collected as they returned from foraging flights and analyzed for pollen and nectar contents. They were subsequently evaluated for expression of LI. Our research revealed that pollen foragers exhibited stronger learning, both in the presence (excitatory conditioning) and absence (LI) of reinforcement. The heightened overall learning ability demonstrated by pollen foragers suggests that pollen foragers are in general more sensitive to a large number of environmental stimuli. This mechanism could contribute toward explanations of colony-level regulation of foraging patterns among workers.Communicated by R. Page     

Colony state and regulation of pollen foraging in the honey bee,Apis mellifera L.

Summary To place social insect foraging behavior within an evolutionary context, it is necessary to establish relationships between individual foraging decisions and parameters influencing colony fitness. To address this problem, we examined interactions between individual foraging behavior and pollen storage levels in the honey bee, Apis mellifera L. Colonies responded to low pollen storage conditions by increasing pollen intake rates 54% relative to high pollen storage conditions, demonstrating a direct relationship between pollen storage levels and foraging effort. Approximately 80% of the difference in pollen intake rates was accounted for by variation in individual foraging effort, via changes in foraging activity and individual pollen load size. An additional 20% resulted from changes in the proportion of the foraging population collecting pollen. Under both high and low pollen storage treatments, colonies returned pollen storage levels to pre-experimental levels within 16 days, suggesting that honey bees regulate pollen storage levels around a homeostatic set point. We also found a direct relationship between pollen storage levels and colony brood production, demonstrating the potential for cumulative changes in individual foraging decisions to affect colony fitness. Offprint requests to: J.H. Fewell at the current address     

Phenotype interactions in group behavior of honey bee workers (Apis mellifera L.)

Summary The alarm reaction of groups of honey bee workers was quantified using a metabolic bioassay. The genetic structure of these groups was varied in order to estimate the effects of worker interactions. Though the group phenotype was mainly determined by additive interactions, nonlinear effects were also found. Mixed worker groups, combined from colonies with similar reactivity in the bioassay, showed a stronger response than pure groups. This phenomenon, analogous to the overdominance model for individuals in classical genetics, has implications for mechanisms of natural and artificial selection in social populations and for the evolution of polyandry in social Hymenoptera.     

氟虫腈对意大利蜜蜂工蜂幼虫及幼龄工蜂的亚致死效应

蜜蜂是重要的授粉昆虫,亦是重要的环境污染指示生物.氟虫腈对蜜蜂剧毒,Pesticide Properties Data Base (PPDB)数据库中登记的其对蜜蜂的急性经口及接触半数致死剂量(LD50)分别为0.00417 μg·蜂-1和0.00597 μg·蜂-1,正因为对非靶标生物的毒性较高,其使用也受到了限制,目前仅用于卫生害虫防治和一些旱田作物的土壤处理等.尽管有关氟虫腈对蜜蜂的危害已有一些报道,但有关其对蜜蜂幼虫和幼龄工蜂的亚致死作用研究仍较为缺乏,鉴于此,本文以意大利蜜蜂(Apis mellifera L.)的工蜂幼虫和新出房工蜂(＜24 h)为研究对象,采用人工饲喂重复染毒法,分别测定了10-3、10-2、0.1、1和10 μg·L-1的氟虫腈对工蜂幼虫的21d慢性毒性和1、5和10 μg·L-1的氟虫腈对新出房工蜂7d和14d的慢性毒性.结果 表明,与对照相比,10-3～ 10 μg·L-1范围内的氟虫腈可以使幼虫化蛹率显著降低20.83％ ～ 47.91％ (P＜0.05),羽化率显著降低25.00％ ～ 43.72％(P＜0.05);对于幼龄工蜂,1μg·L-1和5 μg·L-1氟虫腈暴露7d和14d时蜜蜂死亡率均＜10％;10 μg ·L-1氟虫腈暴露7d时,死亡率＜20％,当暴露时间延长至14 d时,成蜂死亡率高达(65.0± 17.7)％ (P＜0.0001),显著高于对照组,这说明氟虫腈对蜜蜂具有一定的时间累积毒性(time reinforced toxicity,TRT).此外,通过对蜜蜂幼虫和工蜂体内抗氧化酶(超氧化物歧化酶(SOD)、过氧化氢酶(CAT))、解毒酶谷胱甘肽转移酶(GST)酶活力及谷胱甘肽(GSH)、脂质过氧化产物丙二醛(MDA)含量的测定结果表明,氟虫腈暴露可显著提高幼虫体内CAT的酶活力和MDA含量(P＜0.05),但GST的酶活力显著降低(P＜0.01);而成蜂在经过处理后,体内CAT和GST的酶活力、GSH的含量均会显著降低(P＜0.05),这说明亚致死剂量的氟虫腈可干扰蜜蜂机体稳态,引发蜜蜂幼虫和成蜂显著的氧化损伤,从而危害蜜蜂健康.氟虫腈具有较强的内吸特性和环境稳定性,作物种子处理或卫生施用依然可能导致其在花粉、土壤和水体中的痕量级残留,本研究中发现氟虫腈对蜜蜂幼虫和成蜂生存及各生理指标的最低可观察效应浓度(LOEC)可低至10-5 μg·L-1和10 μg·L-1,相关结果可以补充低残留浓度下氟虫腈蜜蜂风险评价数据的不足,为未来氟虫腈的安全用药指导提供参考.     

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.