Choice of flowers by foraging honey bees (Apis mellifera): possible morphological cues

Abstract.

• 1 Honey bees foraging for nectar on lavender (Lavandula stoechas) chose inflorescences with more of their flowers open. The number of open flowers predicted whether an inflorescence was visited by bees, inspected but rejected, or ignored. Inflorescences chosen arbitrarily by observers had numbers of open flowers intermediate between those of visited and ignored inflorescences.
• 2 Differences in morphological characters between types of inflorescence correlated with nectar volume and sugar weight per flower so that visited inflorescences had a disproportionately greater volume of nectar and weight of sugar per flower and greater variance in nectar volume.
• 3 Although there were significant associations between nectar content and the morphological characters of inflorescences, discriminant function analysis revealed discrimination on the basis of morphology rather than nectar content.
• 4 Visited inflorescences tended to have smaller than average flowers but bees tended to probe the largest flowers on visited inflorescences.
• 5 Choice of flowers within inflorescences is explicable in terms of the relationship between flower size and nectar content.

     

Adaptive spatial biases in nectar deposition in the nests of honey bees

Honey bees store their large supply of honey at the top and, to a lesser extent, along the edges of their nests. Whether this pattern is the result of preferences for where nectar is deposited is unclear. Camazine, in a path breaking study of pattern formation, found evidence that workers deposit nectar at random, while Free and Williams in an earlier study found evidence that bees prefer to deposit nectar into particular types of comb. Here we reexamine this question. We tested three hypotheses, all of which posit that bees have adaptive biases which allow them to deposit nectar directly into the most useful locations. We found that bees have preferences for depositing nectar into cells at the top of the nest, into old vs. new comb, and into interior facing comb vs. comb facing the exterior environment. These preferences may ensure that nectar is placed directly into those regions where it will ultimately be stored. They may also result in an optimal pattern of comb usage with respect to brood rearing. This work, along with the results of previous studies, suggests that comb usage patterns may reflect competing selective pressures and be more complicated than previously thought. Received 17 May 2007; revised 15 June 2007; accepted 3 July 2007.     

Genetic variation in worker temporal polyethism and colony defensiveness in the honey bee, Apis mellifera

To test the hypothesis that colonies of honey bees composedof workers with faster rates of adult behavioral developmentare more defensive than colonies composed of workers with slowerbehavioral development, we determined whether there is a correlationbetween genetic variation in worker temporal polyethism andcolony defensiveness. There was a positive correlation for thesetwo traits, both for European and Africanized honey bees. Thecorrelation was larger for Africanized bees, due to differencesbetween Africanized and European bees, differences in experimentaldesign, or both. Consistent with these results was the findingthat colonies with a higher proportion of older bees were moredefensive than colonies of the same size that had a lower proportionof older bees. There also was a positive correlation betweenrate of individual behavioral development and the intensityof colony flight activity, and a negative correlation betweencolony defensiveness and flight activity. This suggests thatthe relationship between temporal polyethism and colony defensivenessmay vary with the manner in which foraging and defense dutiesare allocated among a colony's older workers. These resultsindicate that genotypic differences in rates of worker behavioraldevelopment can influence the phenotype of a honey bee colonyin a variety of ways.     

Effects of Imidacloprid and Varroa destructor on survival and health of European honey bees,Apis mellifera

There has been growing concern over declines in populations of honey bees and other pollinators which are a vital part to our food security. It is imperative to identify factors responsible for accelerated declines in bee populations and develop solutions for reversing bee losses. While exact causes of colony losses remain elusive, risk factors thought to play key roles are ectoparasitic mites Varroa destructor and neonicotinoid pesticides. The present study aims to investigate effects of a neonicotinoid pesticide Imidacloprid and Varroa mites individually on survivorship, growth, physiology, virus dynamics and immunity of honey bee workers. Our study provides clear evidence that the exposure to sublethal doses of Imidacloprid could exert a significantly negative effect on health and survival of honey bees. We observed a significant reduction in the titer of vitellogenin (Vg), an egg yolk precursor that regulates the honey bees development and behavior and often are linked to energy homeostasis, in bees exposed to Imidacloprid. This result indicates that sublethal exposure to neonicotinoid could lead to increased energy usage in honey bees as detoxification is a energy‐consuming metabolic process and suggests that Vg could be a useful biomarker for measuring levels of energy stress and sublethal effects of pesticides on honey bees. Measurement of the quantitative effects of different levels of Varroa mite infestation on the replication dynamic of Deformed wing virus (DWV), an RNA virus associated with Varroa infestation, and expression level of immune genes yields unique insights into how honey bees respond to stressors under laboratory conditions.     

Floral bagging differentially affects handling behaviours and single-visit pollen deposition by honey bees and native bees

1. Measurements of pollinator performance are crucial to pollination studies, enabling researchers to quantify the relative value of different pollinator species to plant reproduction. One of the most widely employed measures of pollinator performance is single-visit pollen deposition, the number of conspecific pollen grains deposited to a stigma after one pollinator visit. To ensure a pollen-free stigma, experimenters must first bag flowers before exposing them to a pollinator. 2. Bagging flowers, however, may unintentionally manipulate floral characteristics to which pollinators respond. In this study, we quantified the effect of bagging on nectar volume in watermelon (Citrullus lanatus) flowers, and how this affects pollinator performance and behaviour. 3. Experimental bagging resulted in roughly 30-fold increases in nectar volume relative to unmanipulated, open-pollinated field flowers after only a few hours. Honey bees, but not native bees, consistently displayed elevated handling times and single-visit pollen deposition on unmanipulated bagged flowers relative to those from which we removed nectar to mimic volumes in open-pollinated flowers. 4. Furthermore, we identify specific bee foraging behaviours during a floral visit that account for differences in pollen deposition, and how these differ between honey bees and native bees. 5. Our findings suggest that experimental bagging of flowers, without accounting for artificially accumulated nectar, can lead to biased estimates of pollinator performance in pollinator taxa that respond strongly to nectar volume. We advise that pollination studies be attentive to nectar secretion dynamics in their focal plant species to ensure unbiased estimates of pollinator performance across multiple pollinator species.     

Comparative resistance in Buckfast and Canadian stocks of honey bees (Apis mellifera L.) to infestation by honey bee tracheal mites (Acarapis woodi (Rennie))

The results of bioassay and colony evaluation demonstrated that British and Texas Buckfast honey bee stocks had one-third to one-half the mean prevalence and abundance of tracheal mites as Canadian standard stock, indicating that Buckfast stocks are less susceptible to tracheal mites than Canadian standard stock. Hybrid Canadian and Buckfast stocks exhibited resistance characteristics similar to only one of their parental stocks, suggesting the colony has an unknown effect on the expression of a bee's resistance to mites. A high correlation (r _s=0.66) between abundance values from the bioassay and colony evaluations indicates that the bioassay can be used to screen bees for mite resistance.     

Departure rules used by bees foraging for nectar: A field test

Summary Departure rules used by solitary long-tongued bees (Anthophora spp. andEucera spp.) collecting nectar from flowers ofAnchusa strigosa (Boraginaceae) were studied. The amount of nectar a bee receives from an individual flower was estimated by measuring the time elapsed since the previous bee visit to that flower. Measurements of nectar accumulation in experimentally emptied flowers indicated that this time interval is an accurate predictor of nectar volumes in flowers. We found that nectar rewards influence the probability of departure from individual plants, as well as distances of movements within plants. The probability of departure from individual plants was negatively related to the amount of reward received at the two lastvisited flowers. This result indicates that the bees used a probabllistic departure rule, rather than a simple threshold departure rule, and that rewards from both the current and the previously visited flower were important in determining departure points. Distances of inter-flower movements within plants were negatively related to the amount of reward received at the current flower. The overall results suggest that the pollinators ofA. strigosa make two types of departure decisions-departures from the whole plant and departures from the neighbourhood of individual flowers-and that they use different departure rules for each scale. Factors influencing the decision-making processes of the observed foraging behaviour are discussed.     

Seasonality of salt foraging in honey bees (Apis mellifera)

1. Honey bees (Apis mellifera) prefer foraging at compound‐rich, ‘dirty’, water sources over clean water sources. As a honey bee's main floral diet only contains trace amounts of micronutrients – likely not enough to sustain an entire colony – it was hypothesised that honey bees forage in dirty water for physiologically essential minerals that their floral diet, and thus the colony, may lack. 2. While there are many studies regarding macronutrient requirements of honey bees, few investigate micronutrient needs. For this study, from 2013 to 2015, a series of preference assays were conducted in both summer and autumn. 3. During all field seasons, honey bees exhibited a strong preference for sodium in comparison to deionised water. There was, however, a notable switch in preferences for other minerals between seasons. 4. Calcium, magnesium, and potassium – three minerals most commonly found in pollen – were preferred in autumn when pollen was scarce, but were avoided in summer when pollen was abundant. Thus, as floral resources change in distribution and abundance, honey bees similarly change their water‐foraging preferences. 5. Our data suggest that, although they are generalists with relatively few gustatory receptor genes, honey bee foragers are fine‐tuned to search for micronutrients. This ability likely helps the foragers in their search for a balanced diet for the colony as a whole.     

Flower visitation patterns of the coexisting honey bees Apis cerana japonica and Apis mellifera (Hymenoptera: Apidae)

We compared flower visitation patterns of two coexisting honey bees, Apis mellifera Linnaeus and Apis cerana japonica Radoszkowski, on 20 plant species, including three exotics, under natural conditions in Nara, Japan, from April to August 2012. We also measured flower color based on bee color vision (15 flower species), nectar volume (nine species) and nectar concentration (eight species). Flowers colored white, pink, red, purple and cream were classified as bee‐blue‐green, and yellow was classified as bee‐green. Apis cerana visited 14 plant species and A. mellifera visited 11. Although the two Apis species are similar in morphology, they visited different plants: in particular, A. cerana visited native plant species more often than did A. mellifera. Both A. mellifera and A. cerana visited not only nectariferous flowers but also those with no nectar. We also found different visitation patterns between A. cerana and A. mellifera: Apis cerana more often visited flowers with smaller color angle (bee‐blue‐green), lower chroma and higher brightness, and flowers secreting nectars of higher concentration and smaller volume than did A. mellifera.     

Identification of a new contingency-based response in honey bees (Apis mellifera) through revision of the proboscis extension conditioning paradigm

The two experiments reported present new information in the area of classical conditioning experiments with honey bees. Experiment 1 establishes a single unconditioned stimulus (US) technique as a preferred technique for conditioning of the proboscis extension response. Experiment 1 further identifies a new head turn response which occurs when the standard compound US technique is used. Experiment 2 demonstrates that the newly identified head turn response is contingency-based and provides important new response to the repertoire of honey bee learning experiments.     

Admixture in Africanized honey bees (Apis mellifera) from Panamá to San Diego,California (U.S.A.)

The Africanized honey bee (AHB) is a New World amalgamation of several subspecies of the western honey bee (Apis mellifera), a diverse taxon historically grouped into four major biogeographic lineages: A (African), M (Western European), C (Eastern European), and O (Middle Eastern). In 1956, accidental release of experimentally bred “Africanized” hybrids from a research apiary in Sao Paulo, Brazil initiated a hybrid species expansion that now extends from northern Argentina to northern California (U.S.A.). Here, we assess nuclear admixture and mitochondrial ancestry in 60 bees from four countries (Panamá; Costa Rica, Mexico; U.S.A) across this expansive range to assess ancestry of AHB several decades following initial introduction and test the prediction that African ancestry decreases with increasing latitude. We find that AHB nuclear genomes from Central America and Mexico have predominately African genomes (76%–89%) with smaller contributions from Western and Eastern European lineages. Similarly, nearly all honey bees from Central America and Mexico possess mitochondrial ancestry from the African lineage with few individuals having European mitochondria. In contrast, AHB from San Diego (CA) shows markedly lower African ancestry (38%) with substantial genomic contributions from all four major honey bee lineages and mitochondrial ancestry from all four clades as well. Genetic diversity measures from all New World populations equal or exceed those of ancestral populations. Interestingly, the feral honey bee population of San Diego emerges as a reservoir of diverse admixture and high genetic diversity, making it a potentially rich source of genetic material for honey bee breeding.     

Adaptive shifts in honey bee (Apis mellifera L.) guarding behavior support predictions of the acceptance threshold model

The acceptance threshold model predicts that in a fluctuatingenvironment a recognition system should be adaptive ratherthan fixed. In particular, discriminating individuals, suchas guards at a nest entrance, should be less permissive toconspecifics when both the frequency of non-nest-mate contact and the cost of accepting non-nest mates is high. We testedthese predictions by studying honey bee guarding during a periodin which nectar conditions changed from dearth to abundance.Initially, during nectar dearth, individual guards accepted80% of introduced nest mates and 25% of non-nest mates. As nectar conditions improved, both the intensity of robbing andguarding and the cost of non-nest-mate acceptance declined.In response, individual guards became more permissive to nestmates and non-nest mates until eventually an "accept-all" thresholdoccurred—all nest mates and non-nest mates were accepted.These data are consistent with a shifting acceptance thresholdand provide the first field data to support the model. A simple linear relationship occurred between the number of guards andthe number of fights, 9:1, observed at the hive entrance, suggestingthat guarding may be regulated by intruder intensity or otherwiseregulated in an adaptive manner.     

Calorimetric investigations of the different castes of honey bees,Apis mellifera carnica

Summary Honey bees of different age and castes were investigated calorimetrically at 20, 25 and 30 °C. Experiments were completed by endoscopic observation of the insects in the visible and the near infrared range and by acoustical monitoring and subsequent frequency analysis of various locomotor activities. Direct calorimetric results of this paper are compared with data of indirect calorimetry from the literature using a respiratory quotient of 1.00 and 21.13 J consumed. Agreements between both methods are generally good. The results show that weight-specific heat production rates increase with age of worker bees by a factor of 5.6 at 30 °C, 3.7 at 25 °C and 40.0 at 20 °C. In groups of foragers the heat production decreases with growing group size to around 6% of the value for an isolated bee. The presence of a fertile queen or of brood reduces the heat output of a small worker group significantly. Adult drones exhibit a much higher metabolic rate (up to 19.7-fold at 20 °C) than juveniles with strong fluctuations in the power-time curves. Fertile queens show a less pronounced heat production rate than virgin queens (54% at 30 °C, 87% at 25 °C and 77% at 20 °C). Calorimetric unrest is much higher for young than for adult queens. Heat production is very low in both uncapped and capped brood and less than 30% of that of a newly emerged worker. In most cases temperature showed a significant influence on the metabolic level, although its sign was not homogeneous between the castes or even within them. Locomotor activities are easily recorded by the acoustic frequency spectrum (0–7.5 kHz) and in good agreement with endoscopic observations and calorimetric traces.Abbreviations RQ respiratory quotient - ww wet weight This paper is part of the PhD thesis of L.F.     

Spatial foraging patterns of the African honey bee,Apis mellifera scutellata

Recruitment patterns were investigated for the African honey bee in the Okavango River Delta, Botswana. The waggle dances of two observation colonies maintained in the field were monitored and used to construct maps of daily recruitment activity. These maps revealed that the African colonies frequently adjusted the allocation of recruits among food patches, recruited for 16–17 different food sites/day over areas of 55–80 km ² ,and concentrated the majority of recruitment within 1 km of the hives (median foraging distances for the two colonies were 295 and 563 m). In both colonies pollen foragers were more abundant than nectar foragers, and pollen sources indicated by waggle dancers were significantly closer to the hives than nectar sources. Compared to the recruitment patterns of temperate climate colonies, the African colonies had smaller recruitment areas, smaller mean recruitment distances, and a greater emphasis on pollen foraging. These differences may be related to the contrasting survival strategies followed by tropical-versus temperate-climate honey bees.     

A modeling approach to swarming in honey bees (Apis mellifera)

Identifying the mechanisms of colony reproduction is essential to understanding the sociobiology of honey bees. Although several proximate causes leading to the initiation of queen rearing – an essential prerequisite to swarming – have been proposed, none have received unequivocal empirical support. Here we model the main proximate hypotheses (colony size, brood comb congestion, and worker age distribution) and show that all proposed swarming triggers occur as a function of the ultimate cause of a colony reaching replacement stability, the point at which the queen has been laying eggs at her maximal rate. We thus present a reproductive optimization model of colony swarming based on evolutionary principles. All models produce results remarkably similar both to each other and to empirically-determined swarming patterns. An examination of the fit between the individual models and swarm-preventing techniques used by beekeepers indicates that the reproductive optimization model has a relatively broad explanatory range. These results suggest that an examination into the behavioral correlates of a queen’s maximum egg laying rate may provide a unified proximate mechanistic trigger leading predictably to colony fission. Generating a predictive model for this very well studied animal is the first step in producing a model of colony fission applicable to other swarm-founding eusocial animals. Received 16 November 2004; revised 31 May 2005; accepted 27 June 2005.     

Intra-colonial variation of the sting extension response in the honey bee Apis mellifera

The workers’ sting extension in response to noxious stimulations is a common test used to study physiological modulations of behaviour in the honey bee. In this study, we investigated the variation of the sting extension response between honey bee workers from different patrilines in a colony with a naturally mated queen. We found that the sting extension response varied according to patrilines, indicating a genetic contribution to the intra-colonial variation of this behaviour. Patrilines differed in their responses during successive stimulations applied at a constant level: bees belonging to some patrilines exhibited a constant level of response during repeated stimulations, while others showed a decreasing response under the same conditions. These results fit well with the models of division of labour based on differences in response thresholds among workers of different subfamilies. This study was carried out in the Laboratoire de Neurobiologie Comparée des Invertébrés (INRA) in Bures-sur-Yvette, France Received 29 April 2005; revised 8 July 2005; accepted 25 July 2005.     

Ovarian control of nectar collection in the honey bee (Apis mellifera)

Honey bees are a model system for the study of division of labor. Worker bees demonstrate a foraging division of labor (DOL) by biasing collection towards carbohydrates (nectar) or protein (pollen). The Reproductive ground-plan hypothesis of Amdam et al. proposes that foraging DOL is regulated by the networks that controlled foraging behavior during the reproductive life cycle of honey bee ancestors. Here we test a proposed mechanism through which the ovary of the facultatively sterile worker impacts foraging bias. The proposed mechanism suggests that the ovary has a regulatory effect on sucrose sensitivity, and sucrose sensitivity impacts nectar loading. We tested this mechanism by measuring worker ovary size (ovariole number), sucrose sensitivity, and sucrose solution load size collected from a rate-controlled artificial feeder. We found a significant interaction between ovariole number and sucrose sensitivity on sucrose solution load size when using low concentration nectar. This supports our proposed mechanism. As nectar and pollen loading are not independent, a mechanism impacting nectar load size would also impact pollen load size.