Solitary and group nesting in the orchid bee <Emphasis Type="Italic">Euglossa hyacinthina</Emphasis> (Hymenoptera,Apidae)

Summary Orchid bees (Euglossini) provide a potentially informative contrast for examining origins of advanced social behaviour in bees because they are the only tribe in the apine clade that do not form large colonies or have queens and workers. We investigated natural nests of Euglossa hyacinthina Dressler, an orchid bee that nests singly or in groups. By comparing the two types of nests, we examined if individuals in a group merely share the nest (are communal) or exhibit a level of social organization where there is reproductive division of labour among the females. Observations are consistent with communal nesting, indicating that all females in group nests are reproductively similar to the solitary nesting females because the provisioning of young, as well as the ovary development and mating status of females sharing nests were not different than that of solitary-nesting females. Also, multiple female nests did not produce a female-biased brood as predicted for nests with reproductive division of labour. We also investigated potential advantages of group nesting vs. individual nesting. We demonstrate that per capita offspring production is lower in nests with more than one female. However, we found that nests with single females were left unattended for longer periods of time during foraging, and that there was a high incidence of natural enemy attack in nests when females were absent. Group and solitary nesting may be advantageous under different conditions.Received 3 December 2002; revised 7 March 2003; accepted 2 April 2003.     

Cryptic plasticity underlies a major evolutionary transition

The origin of eusociality is often regarded as a change of macroevolutionary proportions [1, 2]. Its hallmark is a reproductive division of labor between the members of a society: some individuals ("helpers" or "workers") forfeit their own reproduction to rear offspring of others ("queens"). In the Hymenoptera (ants, bees, wasps), there have been many transitions in both directions between solitary nesting and sociality [2-5]. How have such transitions occurred? One possibility is that multiple transitions represent repeated evolutionary gains and losses of the traits underpinning sociality. A second possibility, however, is that once sociality has evolved, subsequent transitions represent selection at just one or a small number of loci controlling developmental switches between preexisting alternative phenotypes [2, 6]. We might then expect transitional populations that can express either sociality or solitary nesting, depending on environmental conditions. Here, we use field transplants to directly induce transitions in British and Irish populations of the sweat bee Halictus rubicundus. Individual variation in social phenotype was linked to time available for offspring production, and to the genetic benefits of sociality, suggesting that helping was not simply misplaced parental care [7]. We thereby demonstrate that sociality itself can be truly plastic in a hymenopteran.     

Evidence of Entrance Sharing and Subterranean Connections in Andrena agilissima (Hymenoptera; Andrenidae)

Andrena agilissima is a bee that nests on sloped or vertical earth walls. Data from 3 years of fieldwork presented here show that this species is communal and uses the same nesting site for many years. On an earth wall on Isola d'Elba (Tuscany, Italy), covered with many bee nest entrances, we studied an aggregation of Andrena agilissima to determine if bees share entrances, if the sharing provides evidence for subterranean connections, and if bees involved in sharing show a division of labor. We marked several females coming out of the same entrance, as well as recapturing the same females using different entrances. No division of labor was observed in our observations.     

Biogenic amines and division of labor in honey bee colonies: behaviorally related changes in the antennal lobes and age-related changes in the mushroom bodies

Levels of the biogenic amines dopamine, serotonin, and octopamine were measured in different brain regions of adult worker honey bees as a function of age-related division of labor, using social manipulations to unlink age and behavioral state. In the antennal lobes, foragers had higher levels of all three amines than nurses, regardless of age. Differences were larger for octopamine than serotonin or dopamine. In the mushroom bodies, older bees had higher levels of all three amines than younger bees, regardless of behavioral state. These correlative results suggest that increases in octopamine in the antennal lobes may be particularly important in the control of age-related division of labor in honey bees. Accepted: 10 February 1999     

Monitoring circadian rhythms of individual honey bees in a social environment reveals social influences on postembryonic ontogeny of activity rhythms

Social factors constitute an important component of the environment of many animals and have a profound influence on their physiology and behavior. Studies of social influences on circadian rhythms have been hampered by a methodological trade-off: automatic data acquisition systems obtain high-quality data but are effective only for individually isolated animals and therefore compromise by requiring a context that may not be sociobiologically relevant. Human observers can monitor animal activity in complex social environments but are limited in the resolution and quality of data that can be gathered. The authors developed and validated a method for prolonged, automatic, high-quality monitoring of focal honey bees in a relatively complex social environment and with minimal illumination. The method can be adapted for studies on other animals. The authors show that the system provides a reliable estimation of the actual path of a focal bee, only rarely misses its location for > 1 min, and removes most nonspecific signals from the background. Using this system, the authors provide the first evidence of social influence on the ontogeny of activity rhythms. Young bees that were housed with old foragers show ~24-h rhythms in locomotor activity at a younger age and with stronger rhythms than bees housed with a similar number of young bees. By contrast, the maturation of the hypopharyngeal glands was slower in bees housed with foragers, similar to findings in previous studies. The morphology and function of the hypopharyngeal glands vary along with age-based division of labor. Therefore, these findings indicate that social inhibition of task-related maturation was effective in the experimental setup. This study suggests that although the ontogeny of circadian rhythms is typically correlated with the age-based division of labor, their social regulation is different.     

Biogenic amines and division of labor in honey bee colonies

Brain levels of dopamine, serotonin, and octopamine were measured in relation to both age-related division of labor and inter-individual differences in task specialization independent of age in honey bee colonies. The only differences among similarly aged bees performing different tasks were significantly lower levels of dopamine in food storers than comb builders and significantly lower levels of octopamine in soldiers than foragers, but soldiers also were slightly younger than foragers. Differences associated with age-related division of labor were stronger. Older bees, notably foragers, had significantly higher levels of all three amines than did younger bees working in the hive. Using social manipulations to unlink chronological age and behavioral status, octopamine was found to exhibit the most robust association between behavior and amine level, independent of age. Octopamine levels were significantly lower in normal-age nurses versus precocious foragers and overage nurses versus normal-age foragers, but not different in reverted nurses versus reversion colony foragers. Dopamine levels were significantly lower in normal-age nurses versus precocious foragers, but higher in reverted nurses versus reversion colony foragers. Serotonin levels did not differ in any of these comparisons. These correlative results suggest that octopamine is involved in the regulation of age-related division of labor in honey bees. Accepted: 10 February 1999     

Juvenile hormone and circadian locomotor activity in the honey bee Apis mellifera

Age-related division of labor in honeybees is associated with plasticity in circadian rhythms. Young nest bees care for brood around the clock with no circadian rhythms while older foragers have strong circadian rhythms that are used for sun compass navigation and for timing visits to flowers. Since juvenile hormone (JH) is involved in the coordination of physiological and behavioral processes underlying age-related division of labor in honey bees, we tested the hypothesis that JH influences the ontogeny of circadian rhythms and other clock parameters in young worker bees. Treatments with the JH analog methoprene or allatectomy did not influence the onset of rhythmicity, overall locomotor activity, or the free-running period of rhythmic locomotor behavior. There were, however, significant differences in the onset of rhythmicity, overall locomotor activity, and longevity between bees from different source colonies, suggesting that there is significant genetic variation for these traits. Our results suggest that JH does not coordinate all aspects of division of labor in bees and that coordination of task performance with circadian rhythms is probably mediated by other regulatory systems.     

Nesting aggregation as a predictor of brood parasitism in mason bees (Osmia spp.)

1. Parasitism can be an important source of mortality for insect populations; however, we know little about the factors influencing vulnerability of wild bees to parasites. Mason bees (genus Osmia; Hymenoptera: Megachilidae) are important pollinators of crops and wild plants and are vulnerable to attack by brood parasites. High nest densities may increase rates of brood parasitism by attracting disproportionate numbers of parasites. 2. Three years of field observations from multiple sites were analysed to assess whether mason bee brood parasitism increased with host density. Mason bees were allowed to nest in artificial nesting blocks and establish natural variation in nesting density. Nest cells constructed by bees were checked for the presence of parasite eggs. 3. Parasitism of nest cells strongly increased with the number of actively nesting bees at a nesting block. Mason bees showed no preference for nesting in blocks that were occupied or unoccupied by other mason bees. Parasitism also increased with the number of days a nest was provisioned and decreased over the course of the season. Nest cells constructed last in a nest were significantly more parasitised than inner cells, despite being sealed against invasions. 4. These findings show positively density‐dependent parasitism in mason bees. They also suggest that bees terminate parasitised nests, causing parasitised cells to become outermost nest cells – a behaviour that may represent a defence against parasites. Our results have implications for the management of mason bees as agricultural pollinators, as cultivating them at high densities could reduce offspring survival.     

Division of Labor Associated with Brood Rearing in the Honey Bee: How Does It Translate to Colony Fitness?

Division of labor is a striking feature observed in honey bees and many other social insects. Division of labor has been claimed to benefit fitness. In honey bees, the adult work force may be viewed as divided between non-foraging hive bees that rear brood and maintain the nest, and foragers that collect food outside the nest. Honey bee brood pheromone is a larval pheromone that serves as an excellent empirical tool to manipulate foraging behaviors and thus division of labor in the honey bee. Here we use two different doses of brood pheromone to alter the foraging stimulus environment, thus changing demographics of colony division of labor, to demonstrate how division of labor associated with brood rearing affects colony growth rate. We examine the effects of these different doses of brood pheromone on individual foraging ontogeny and specialization, colony level foraging behavior, and individual glandular protein synthesis. Low brood pheromone treatment colonies exhibited significantly higher foraging population, decreased age of first foraging and greater foraging effort, resulting in greater colony growth compared to other treatments. This study demonstrates how division of labor associated with brood rearing affects honey bee colony growth rate, a token of fitness.     

Sensory response system of social behavior tied to female reproductive traits

Background

Honey bees display a complex set of anatomical, physiological, and behavioral traits that correlate with the colony storage of surplus pollen (pollen hoarding). We hypothesize that the association of these traits is a result of pleiotropy in a gene signaling network that was co-opted by natural selection to function in worker division of labor and foraging specialization. By acting on the gene network, selection can change a suite of traits, including stimulus/response relationships that affect individual foraging behavior and alter the colony level trait of pollen hoarding. The ‘pollen-hoarding syndrome’ of honey bees is the best documented syndrome of insect social organization. It can be exemplified as a link between reproductive anatomy (ovary size), physiology (yolk protein level), and foraging behavior in honey bee strains selected for pollen hoarding, a colony level trait. The syndrome gave rise to the forager-Reproductive Ground Plan Hypothesis (RGPH), which proposes that the regulatory control of foraging onset and foraging preference toward nectar or pollen was derived from a reproductive signaling network. This view was recently challenged. To resolve the controversy, we tested the associations between reproductive anatomy, physiology, and stimulus/response relationships of behavior in wild-type honey bees.

Methodology/Principal Findings

Central to the stimulus/response relationships of honey bee foraging behavior and pollen hoarding is the behavioral trait of sensory sensitivity to sucrose (an important sugar in nectar). To test the linkage of reproductive traits and sensory response systems of social behavior, we measured sucrose responsiveness with the proboscis extension response (PER) assay and quantified ovary size and vitellogenin (yolk precursor) gene expression in 6–7-day-old bees by counting ovarioles (ovary filaments) and by using semiquantitative real time RT-PCR. We show that bees with larger ovaries (more ovarioles) are characterized by higher levels of vitellogenin mRNA expression and are more responsive to sucrose solutions, a trait that is central to division of labor and foraging specialization.

Conclusions/Significance

Our results establish that in wild-type honey bees, ovary size and vitellogenin mRNA level covary with the sucrose sensory response system, an important component of foraging behavior. This finding validates links between reproductive physiology and behavioral-trait associations of the pollen-hoarding syndrome of honey bees, and supports the forager-RGPH. Our data address a current evolutionary debate, and represent the first direct demonstration of the links between reproductive anatomy, physiology, and behavioral response systems that are central to the control of complex social behavior in insects.     

野生蜜蜂及其传粉作用的研究现状

传粉是维持与提升生物多样性的重要生态过程。膜翅目蜜蜂总科昆虫是自然界中最重要的传粉者, 但对野生蜜蜂的研究一直以来非常薄弱, 如野生蜜蜂类群的资源调查、种类的准确鉴别、营巢生物学与传粉生物学研究等方面。目前, 生物多样性与保护生物学方面的工作越来越多地涉及野生蜜蜂与植物的相互关系, 地方植物区系与农林作物的传粉生物学基础研究与应用项目也引起重视。本文综述了国内外野生蜜蜂的研究现状, 期望从分类学、营巢生物学与传粉生物学等方面推动野生蜜蜂传粉在农林业生产实践中的应用。     

木蜂的巢内行为和交配策略

木蜂Xylocopa作为蜜蜂科的一个重要类群, 用来研究昆虫社会进化早期阶段具有重要意义。本文综述了近年来木蜂的营巢习性、 社会性行为和交配策略的研究进展。木蜂巢的建筑与巢内巢室的分布、 巢室的大小、 贮备蜂粮的效率和被寄生的敏感性等均有一定的关系。在筑巢地点, 随着木蜂种群数量的增加, 同种雌蜂之间的资源存在着竞争, 木蜂对巢室的守卫加强, 更多地表现为对同种雌蜂的守卫以及防御其他的天敌入侵。其社会多态性由独栖性向社会性演化, 主要表现为独栖性、 亚社会性、 半社会性、 共生性和准社会性等方式, 甚至同一种群内会出现不同的社会性行为。在交配策略上, 木蜂的雄蜂在外部形态特征上具有适应交配和寻找雌蜂的进化特征, 并且具有复杂的领地行为。这些研究理论对于我们深刻理解木蜂的行为生物学具有重要意义, 同时也有助于进行更深层次的社会性蜂类演化进程的探索。     

A Strong Immune Response in Young Adult Honeybees Masks Their Increased Susceptibility to Infection Compared to Older Bees

Honeybees, Apis mellifera, show age-related division of labor in which young adults perform maintenance (“housekeeping”) tasks inside the colony before switching to outside foraging at approximately 23 days old. Disease resistance is an important feature of honeybee biology, but little is known about the interaction of pathogens and age-related division of labor. We tested a hypothesis that older forager bees and younger “house” bees differ in susceptibility to infection. We coupled an infection bioassay with a functional analysis of gene expression in individual bees using a whole genome microarray. Forager bees treated with the entomopathogenic fungus Metarhizium anisopliae s.l. survived for significantly longer than house bees. This was concomitant with substantial differences in gene expression including genes associated with immune function. In house bees, infection was associated with differential expression of 35 candidate immune genes contrasted with differential expression of only two candidate immune genes in forager bees. For control bees (i.e. not treated with M. anisopliae) the development from the house to the forager stage was associated with differential expression of 49 candidate immune genes, including up-regulation of the antimicrobial peptide gene abaecin, plus major components of the Toll pathway, serine proteases, and serpins. We infer that reduced pathogen susceptibility in forager bees was associated with age-related activation of specific immune system pathways. Our findings contrast with the view that the immunocompetence in social insects declines with the onset of foraging as a result of a trade-off in the allocation of resources for foraging. The up-regulation of immune-related genes in young adult bees in response to M. anisopliae infection was an indicator of disease susceptibility; this also challenges previous research in social insects, in which an elevated immune status has been used as a marker of increased disease resistance and fitness without considering the effects of age-related development.     

Octopamine influences division of labor in honey bee colonies

Forager honey bees have higher brain levels of octopamine than do bees tending larvae in the hive. To test the hypothesis that octopamine influences honey bee division of labor we treated bees orally with octopamine or its immediate precursor tyramine and determined whether these treatments increased the probability of initiating foraging. Octopamine treatment significantly elevated levels of octopamine in the brain and caused a significant dose-dependent increase in the number of new foragers. This effect was seen for precocious foragers in single-cohort colonies and foragers in larger colonies with more typical age demographies. Tyramine treatment did not increase the number of new foragers, suggesting that octopamine was exerting a specific effect. Octopamine treatment was effective only when given to bees old enough to forage, i.e., older than 4 days of age. Treatment when bees were 1-3 days of age did not cause a significant increase in the number of new foragers when the bees reached the minimal foraging age. These results demonstrate that octopamine influences division of labor in honey bee colonies. We speculate that octopamine is acting in this context as a neuromodulator.     

Percent lipid is associated with body size but not task in the bumble bee <Emphasis Type="Italic">Bombus impatiens</Emphasis>

In some group-living organisms, labor is divided among individuals. This allocation to particular tasks is frequently stable and predicted by individual physiology. Social insects are excellent model organisms in which to investigate the interplay between physiology and individual behavior, as division of labor is an important feature within colonies, and individual physiology varies among the highly related individuals of the colony. Previous studies have investigated what factors are important in determining how likely an individual is, compared to nestmates, to perform certain tasks. One such task is foraging. Corpulence (i.e., percent lipid) has been shown to determine foraging propensity in honey bees and ants, with leaner individuals being more likely to be foragers. Is this a general trend across all social insects? Here we report data analyzing the individual physiology, specifically the percent lipid, of worker bumble bees (Bombus impatiens) from whom we also analyze behavioral task data. Bumble bees are also unusual among the social bees in that workers may vary widely in size. Surprisingly we find that, unlike other social insects, percent lipid is not associated with task propensity. Rather, body size closely predicts individual relative lipid stores, with smaller worker bees being allometrically fatter than larger worker bees.     

Sucrose response thresholds of honey bee (Apis mellifera) foragers are not modulated by brood ester pheromone

Division of labor is a hallmark of eusocial insects and their ecological success can be attributed to it. Honey bee division of labor proceeds along a stereotypical ontogenetic path based on age, modulated by various internal and external stimuli. Brood pheromone is a major social pheromone of the honey bee that has been shown to affect honey bee division of labor. It elicits several physiological and behavioral responses; notably, regulating the timing of the switch from performing in-hive tasks to the initiation of foraging. Additionally, brood pheromone affects future foraging choice. In honey bees, sucrose response threshold is a physiological correlate of age of first foraging and foraging choice. Brood pheromone has been shown to modulate sucrose response threshold in young bees, but its effects on sucrose response thresholds of bees in advanced behavioral states (foragers) are not known. In this study we examined the sucrose response thresholds of two different task groups, foragers (pollen and non-pollen) and non-foraging bees, in response to honey bee brood pheromone. Sucrose response thresholds were not significantly different between brood pheromone treatment and controls among both non-pollen and pollen foragers. However, the sucrose response threshold of non-foraging bees was significantly higher in the brood pheromone treatment group than in the control group. The switch to foraging task is considered a terminal one, with honey bee lifespan being determined at least partially by risks and stress accompanying foraging. Our results indicate that foragers are physiologically resistant to brood pheromone priming of sucrose response thresholds.     

Comparison of social and solitary nesting carpenter bees in sympatry reveals no advantage to social nesting

Facultatively social bees allow for comparisons of social and solitary behaviour under similar environmental conditions. When such bees are polymorphic within the same population it provides a special and somewhat unusual opportunity to examine factors leading to cooperative (social) behaviours where many parameters such as environment are not variable. Some species of bees in the genus Xylocopa offers such opportunities. Studies of these bees often point to guarding and resource limitation as factors leading to social nesting. The large carpenter bee Xylocopa virginica L. (Hymenoptera: Apidae) is one species that exhibits both solitary and social nesting behaviour within the same populations. This paper first compares social and solitary nests in an Ontario population of X. virginica to determine if there is a reproductive advantage to social nesting. Following this, a series of possible explanations for social nesting, and the roles of females in social nests are examined. Social nests have similar brood sizes to solitary nests and productivity as a function of colony size is reduced with increasing number of foundresses. Additional foundresses are not effective guards, do not prevent parasitism, do not likely perform significant work, and do not assume foraging with the loss of a primary foundress. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 998–1010.     

Physiological correlates of division of labor among similarly aged honey bees

Hormone analyses and exocrine gland measurements were made to probe for physiological correlates of division of labor among similarly aged adult worker honey bees (Apis mellifera L.). Middle-age bees (ca. 2 weeks old) performing different tasks showed significant differences in both juvenile hormone (JH) biosynthesis rates and hemolymph titers; guards and undertakers had high JH, and wax producers and food storers, low JH. Guards and undertakers had similar hormone levels to foragers, even though they were 10 days younger than foragers. No differences in JH were detected among young bees (1-week-old queen attendants and nurses) or older bees (3–4 week-old pollen foragers, non-pollen foragers, and soldiers). Hypopharyngeal gland size was inversely correlated with worker age and rate of JH biosynthesis, but soldiers had significantly larger hypopharyngeal glands than did foragers, despite their similar age and JH level. Results from soldiers indicate that exocrine gland development is not always linked with age-related behavior and endocrine development; they also support the recent claim that soldiers constitute a group of older bees that are distinct from foragers. Hormonal analyses indicate that the current model of JH's role in honey bee division of labor needs to be expanded because high levels of JH are associated with several other tasks besides foraging. JH may be involved in the regulation of division of labor among similarly aged workers in addition to its role in age-related division of labor.Abbreviations JH Juvenile hormone - RIA radioimmunoassay - CA corpora allata - HPLC high performance liquid chromatography - TLC thin layer chromatography     

period expression in the honey bee brain is developmentally regulated and not affected by light, flight experience, or colony type

Changes in circadian rhythms of behavior are related to age-based division of labor in honey bee colonies. The expression of the clock gene period (per) in the bee brain is associated with age-related changes in circadian rhythms of behavior, but previous efforts to firmly associate per brain expression with division of labor or age have produced variable results. We explored whether this variability was due to differences in light and flight experience, which vary with division of labor, or differences in colony environment, which are known to affect honey bee behavioral development. Our results support the hypothesis that per mRNA expression in the bee brain is developmentally regulated. One-day-old bees had the lowest levels of expression and rarely showed evidence of diurnal fluctuation, while foragers and forager-age bees (> 21 days of age) always had high levels of brain per and strong and consistent diurnal patterns. Results from laboratory and field experiments do not support the hypothesis that light, flight experience, and colony type influence per expression. Our results suggest that the rate of developmental elevation in per expression is influenced by factors other than the ones studied in our experiments, and that young bees are more sensitive to these factors than foragers.     

Nesting success of wood‐cavity‐nesting bees declines with increasing time since wildfire

Bees require distinct foraging and nesting resources to occur in close proximity. However, spatial and temporal patterns in the availability and quantity of these resources can be affected by disturbances like wildfire. The potential for spatial or temporal separation of foraging and nesting resources is of particular concern for solitary wood‐cavity‐nesting bees as they are central‐place, short‐distance foragers once they have established their nest. Often the importance of nesting resources for bees have been tested by sampling foraging bees as a proxy, and nesting bees have rarely been studied in a community context, particularly postdisturbance. We tested how wood‐cavity‐nesting bee species richness, nesting success, and nesting and floral resources varied across gradients of wildfire severity and time‐since‐burn. We sampled nesting bees via nesting boxes within four wildfires in southwest Montana, USA, using a space‐for‐time substitution chronosequence approach spanning 3–25 years postburn and including an unburned control. We found that bee nesting success and species richness declined with increasing time postburn, with a complete lack of successful bee nesting in unburned areas. Nesting and floral resources were highly variable across both burn severity and time‐since‐burn, yet generally did not have strong effects on nesting success. Our results together suggest that burned areas may provide important habitat for wood‐cavity‐nesting bees in this system. Given ongoing fire regime shifts as well as other threats facing wild bee communities, this work helps provide essential information necessary for the management and conservation of wood‐cavity‐nesting bees.