Foraging dynamics of bumble bees: correlates of movements within and between plant species

What rules determine whether bumble bees continue exploitingplants of the species just visited or switch to another species?To tackle this question, we recorded handling times and flighttimes from bees foraging in a natural meadow containing fiveplant species. Inter- and intra-specific plant distances werequantified. The bee-subjective colors of the five species weredetermined; two of these species had similar colors and structures,while three species were distinct from all others. The followingrules were identified: (1) The decision to switch species wascorrelated with previous flower handling time, which we assumeis a function of the reward amount received at the flower. Aftershort handling times, the probability of switching to anotherspecies increased, whereas it decreased after long handlingtimes. This difference became even greater if the bee had hada run of several short or several long handling times. (2) Constantflights (those between flowers of the same species) and transitionflights (those between flowers of different species) followedstereotyped temporal patterns independent of the distances betweenflowers. Constant flights within five plant species consistentlyhad median durations of about 2 seconds, whereas median transitiontimes between species took 3–6 seconds. (3) This temporalrule broke down, however, if the flowers of two species hadsimilar colors, in which case transition flights had equal dynamicsas constant flights. (4) Bees switched more frequently fromrare than from common species but even more frequently betweensimilar species. We conclude that the bees' choices were determinedby a set of rules that guided them to stay with the currentplant species as long as flowers were rewarding and availablewithin close distance but to switch to another species if flowersoffered low rewards or were not encountered at close range     

Contrasting movement patterns of nectar-collecting and pollen-collecting bumble bees (Bombus terricola) on fireweed (Chamaenerion angustifolium) inflorescences

Abstract. 1. Movements of nectar and pollen-foraging bumble bees on inflorescences of Chamaenerion angustifolium (L.) J. Holub (fireweed or rosebay willow herb) were compared with predictions based on reward distributions and optimality principles. Observations suggest that nectar and pollen-gathering bumble bees behave according to the same set of reward maximization criteria when foraging from flowers of this species.
2. Both kinds of foragers matched their arrival points with the vertical positions on inflorescences in which the densities of their respective food resources were greatest. For nectar-foragers, this point was located at the lowest tier of flowers, whereas for pollen-foragers it was found in the middle of the inflorescences. Nectar and pollen-foraging bees both moved upward on inflorescences following gradients from high to low reward availability.
3. Nectar-foragers responded to decreases in inflorescence size over the season by reducing the number of flower visits made on each raceme. Number of flowers visited by pollen-foragers was low throughout and reflected the scarcity of male-phase flowers on racemes. Flower revisitation rates were low for both kinds of workers, but were slightly higher for those collecting pollen.     

Recognition of incomplete patterns by bumble bees

Bumble bees were trained to discriminate between two visual patterns, one of which was rewarding (S+) and one of which was unrewarding (S-). Subsequently, they were tested for discrimination between two non-rewarding patterns: the top halves of the training patterns, the bottom halves or the side halves. Three conditions were tested: (1) When the S+ was a star and the S- was a circle, all halves of the star were chosen above chance level, which may reflect an unlearned preference for radial patterns. (2) When the S+ and S- were reversed, the bottom half and the side half of the circle were chosen above chance level, but not the top half. (3) In the last condition, the S+ was again a circle, but the feeder tube was placed below the training pattern rather than above, and again the bottom halves were discriminated but neither the top nor the side halves were. In learning pattern discriminations, the ventral portion of the pattern is weighted more strongly than the dorsal portion, which enables recognition of incomplete patterns, and the weighting depends little on angle of approach.     

Non-lethal sampling of DNA from bumble bees for conservation genetics

Summary Non-lethal sampling of DNA from individuals in wild populations will often be required for studies of the conservation genetics of social insects, since it avoids destroying members of scarce or declining species. We investigated the effectiveness and consequences of methods of non-lethal sampling of DNA from bumble bee workers. In an experiment with two captive and confined Bombus terrestris colonies, we found that, unlike sampling haemolymph, sampling the terminal portion of the tarsus of a mid-leg of a worker reliably yielded amplifiable microsatellite DNA and did not significantly reduce worker survivorship. In a further experiment with four B. terrestris colonies whose workers were allowed to forage freely at flowers in the external environment, tarsal sampling of either a mid-leg or a hind-leg had no significant effects on worker survivorship, the mean body mass of foraging workers, the frequency or duration of foraging trips, mass of pollen loads or mass of nectar loads. We therefore suggest that tarsal sampling of either a mid-leg or a hind-leg is an effective and acceptable means of non-lethally sampling DNA from workers in wild populations of bumble bees, because effects on individual and colony performance are likely to be absent or minimal.Received 2 December 2002; revised 10 April 2003; accepted 25 April 2003.     

Experimental analyses of competition between two species of bumble bees (Hymenoptera: apidae)

Summary Dynamical aspects of flower usage and forager body size in sympatric and experimentally-induced allopatric populations of Bombus flaviforns and Bombus rufocinctus were studied in 10 discrete subalpine meadows and over the last half of one summer. Results indicate that there is a high degree of asymmetry in the competitive effects and that B. flavifrons is the clear competitive and numerical dominant. When occurring alone, B. rufocinctus used the same spectrum of flowers in similar frequencies to that of B. flavifrons whose flower use was invariant over all meadows and treatments. When sympatric with B. flavifrons, B. rufocinctus was relegated to secondary, less preferred flowers. Shifts in flower use by B. rufocinctus were accompanied by changes in forager body-size: body weights were greater in allopatric populations of B. rufocinctus and smaller in those sympatric with B. flavifrons. Competitive dominance may be related to differences in species phenologies. Bombus flavifrons initiated colonies in the spring three weeks before B. rufocinctus and maintained higher densities over the summer; by virtue of greater numbers of foragers, it may control exploitation of the most profitable flowers.     

Olfactory conditioning of the proboscis extension in bumble bees

The foraging behaviour of bumble bees is well documented for nectar and/or pollen gathering, but little is known about the learning processes underlying such behaviour. We report olfactory conditioning in worker bumble bees Bombus terrestris L. (Hymenoptera: Apidae) obtained under laboratory conditions on restrained individuals. The protocol was adapted from the proboscis extension conditioning previously described in the honey bee Apis mellifera L. Bumble bees were found to be able to learn a pure odorant when it was presented in paired association with a sugar reward, but not when odour and reward were presented in an explicitly unpaired procedure. This suggests an associative basis for this olfactory learning. Bumble bees showed similar conditioning abilities when stimulated with two different floral odours. An effect of the sugar reward concentration on the learning performances was found.     

Colour choices of naive bumble bees and their implications for colour perception

The innate preferences of inexperienced bumble bees, Bombus terrestris, for floral colour stimuli were studied using artificial flowers. The artificial flowers provided a colour pattern and consisted of a star-shaped corolla and of central colour patches similar to the nectar guide of natural flowers. The innate choice behaviour was assessed in terms of the number of approach flights from some distance towards the artificial flowers and the percentage of approach flights terminating in antennal contact with the floral guide. The colours of the floral guide, the corolla and the background were varied. It was shown that the innate flower colour preference in bumble bees has two components. 1. The frequency of approaches from a distance is correlated with the colour difference between the corolla and the background against which it is presented. If the corolla colour was constant but its background colour varied, the relative attractiveness of the corolla increased with its colour difference to the background. The colour difference assessment underlying this behaviour on a perceptual basis can be attained by means of colour opponent coding, a system well-established in Hymenoptera. 2. The frequency of antennal contacts with the floral guides relative to that of approach flights cannot be accounted for by colour opponent coding alone. Whether the approach flights are interrupted, or whether they end in an antennal contact with the nectar guide is strongly dependent on the direction (sign) of the colour difference, not only its magnitude. The choice behaviour requires a unique perceptual dimension, possibly that of colour saturation or that of hue perception comparable to components of colour perception in humans.     

Effective paternity in natural colonies of Japanese native bumble bees

Kin selection theory predicts a high coefficient of genetic relatedness among nestmates, explaining the frequent evolution of eusociality in a social hymenopteran colony. The bumble bee is a primitively eusocial hymenoptera whose colonies are founded by a single queen. In such a monogynous colony, mating frequency of the queen is the sole factor that affects genetic relatedness among nestmates. Although the queens of most bumble bee species are known to be monandrous, there are some species that are known to be polyandrous. Here, we estimated the effective paternity in the native colonies of Japanese bumble bees, Bombus ardens, B. diversus, and B. honshuensis, using genetic polymorphic data of microsatellites. We found no evidence for polyandry in any investigated colonies, which suggests that within-colony genetic relatedness is very high for all of these colonies.     

Differential sensitivity of honey bees and bumble bees to a dietary insecticide (imidacloprid)

Currently, there is concern about declining bee populations and the sustainability of pollination services. One potential threat to bees is the unintended impact of systemic insecticides, which are ingested by bees in the nectar and pollen from flowers of treated crops. To establish whether imidacloprid, a systemic neonicotinoid and insect neurotoxin, harms individual bees when ingested at environmentally realistic levels, we exposed adult worker bumble bees, Bombus terrestris L. (Hymenoptera: Apidae), and honey bees, Apis mellifera L. (Hymenoptera: Apidae), to dietary imidacloprid in feeder syrup at dosages between 0.08 and 125 μg l^?1. Honey bees showed no response to dietary imidacloprid on any variable that we measured (feeding, locomotion and longevity). In contrast, bumble bees progressively developed over time a dose-dependent reduction in feeding rate with declines of 10–30% in the environmentally relevant range of up to 10 μg l^?1, but neither their locomotory activity nor longevity varied with diet. To explain their differential sensitivity, we speculate that honey bees are better pre-adapted than bumble bees to feed on nectars containing synthetic alkaloids, such as imidacloprid, by virtue of their ancestral adaptation to tropical nectars in which natural alkaloids are prevalent. We emphasise that our study does not suggest that honey bee colonies are invulnerable to dietary imidacloprid under field conditions, but our findings do raise new concern about the impact of agricultural neonicotinoids on wild bumble bee populations.     

Effects of recent experience on foraging decisions by bumble bees

The temporal and spatial scales employed by foraging bees in sampling their environment and making foraging decisions should depend both on the limits of bumble bee memory and on the spatial and temporal pattern of rewards in the habitat. We analyzed data from previous experiments to determine how recent foraging experience by bumble bees affects their flight distances to subsequent flowers. A single visit to a flower as sufficient to affect the flight distance to the next flower. However, longer sequences of two or three visits had an additional effect on the subsequent flight distance of individual foragers. This suggests that bumble bees can integrate information from at least three flowers for making a subsequent foraging decision. The existence of memory for floral characteristics at least at this scale may have significance for floral selection in natural environments.     

Estimating colony locations of bumble bees with moving average model

It is very difficult to find natural colonies of bumble bees in the field. In this study, the yearly dynamics of floral resources and foraging bumble bee workers were investigated. The optimal colony locations were estimated from the data using moving average on the assumption that bumble bee queens and workers were omniscient. Fortunately, a colony of Bombus ardens was found, and the true location of the colony was evaluated with the estimated optimal locations. The true location was optimal at the latter half of the breeding season.An erratum to this article can be found at     

A comprehensive phylogeny of the bumble bees (Bombus)

Bumble bees ( Bombus Latreille) occupy a wide diversity of habitats, from alpine meadows to lowland tropical forest, yet they appear to be similar in morphology throughout their range, suggesting that behavioural adaptations play a more important role in colonizing diverse habitats. Notwithstanding their structural homogeneity, bumble bees exhibit striking inter- and intraspecific variation in colour pattern, purportedly the outcome of mimetic evolution. A robust phylogeny of Bombus would provide the framework for elucidating the history of their wide biogeographical distribution and the evolution of behavioural and morphological adaptations, including colour pattern. However, morphological studies of bumble bees have discovered too few phylogenetically informative characters to reconstruct a robust phylogeny. Using DNA sequence data, we report the first nearly complete species phylogeny of bumble bees, including most of the 250 known species from the 38 currently recognized subgenera. Bayesian analysis of nuclear (opsin, EF-1α, arginine kinase, PEPCK) and mitochondrial (16S) sequences results in a highly resolved and strongly supported phylogeny from base to tips, with clear-cut support for monophyly of most of the conventional morphology-based subgenera. Most subgenera fall into two distinct clades ( short-faced and long-faced ) associated broadly with differences in head morphology. Within the short-faced clade is a diverse New World clade, which includes nearly one-quarter of the currently recognized subgenera, many of which are restricted to higher elevations of Central and South America. The comprehensive phylogeny provides a firm foundation for reclassification and for evaluating character evolution in the bumble bees.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 161–188.     

Competition between hummingbirds and bumble bees for nectar in flowers of Impatiens biflora

Summary Using removal experiments and concurrent measurement of resource levels, evidence was obtained for exploitation competition between Ruby-throated hummingbirds and two bumble bee species (Bombus fervidus and B. vagans) foraging for nectar on Impatiens biflora.When all three species were active, flower visitors showed a complex pattern of resource partitioning involving both diel and spatial changes. Hummingbirds foraged almost exclusively from the outermost exposed flowers on plants from which they drained nectar levels beyond the reach of bees over most of the day. In contrast the longtongued bee species (B. fervidus), and the shorter-tongued B. vagans, displayed a preference for the innermost flowers on plants which were protected from hummingbird visitation by surrounding vegetation. The two Bombus spp. began foraging at different times during the day: B. vagans were most active in early morning but were replaced by B. fervidus later in the day.When hummingbirds were rare, only B. fervidus showed evidence of competitive release: an increase in the number of foragers and a broadening of flower choice to include more outer flowers. Workers of B. vagans showed a similar response to temporary removal of B. fervidus and also extended their foraging over the entire day. These responses were consistent with changes in the availability of nectar to different species.Removal experiments demonstrated that individuals of one species can be largely excluded from access to nectar resources as a direct result of exploitation of nectar by foragers of other species with longer tongues. Thus in this system interspecific exploitation is an important mechanism involved in resource partitioning.     

The turnover of milkweed pollinia on bumble bees,and implications for outcrossing

Summary Bumble bees (Bombus spp.) picked up a pollen packet (pollinium) of milkweed (Asclepias syriaca L.) every 2–5 h, usually more rapidly on their feet than on their mouthparts. Pollinia were retained an average of slightly over one day on the mouthparts and one-quarter day on the feet. This long retention period enhances the possibility of outcrossing in this largely or completely self-incompatible species. Although many more pollinia were carried on the feet, the longer retention of those on the mouthparts resulted in their collective outcrossing potential exceeding that of pollinia on the feet. Once pollinia became attached to the bees (via their attachment mechanisms, the corpuscula), others often attached to the translator arms (connecting corpusculum with pollinia) of the first pollinia. Long strings of pollinia and corpuscula often resulted, but they frequently were shed down to a single corpusculum, which was usually retained for long periods (estimated retention time=12–43 days). During the middle and latter part of the flowering period about two-thirds of the bees' feet carried only a single corpusculum. Feet in this condition picked up extremely few pollinia and thus were largely unavailable as sites for pollen transfer. Having several single corpuscula on the feet greatly lowered the number of pollinia carried by a bee over the season. Single corpuscula occurred much less frequently on the mouthparts and were shed over 25 times as rapidly as those on the feet. Many more bumble bees moved between clones than did other possible diurnal pollinators, largely a result of being several times more abundant than all other visitors combined. This factor, plus their heavy pollinia load, suggests that they were the most important diurnal pollinators of these clones.     

The effect of nectar abundance on foraging patterns of bumble bees

Abstract.

• 1 Bumble bees (Bombus spp.) fed more on previously screened, nectar-rich plots of cow vetch (Vicia cracca) and white clover (Trifolium repens), and remained longer on inflorescences there, than on continually-exploited plots of these flowers. No significant differences between previously screened and continually available plots occurred in the number of individuals visiting these two areas, the number of inflorescences per visit, the number of florets visited per inflorescence, and the percentage of inflorescences rejected.
• 2 Individual bees were analysed in greater detail. They visited more inflorescences and spent longer times on cow vetch in the previously-screened plots, whether moving from previously-screened to continually available areas, or vice versa. On white clover the same pattern held for bees moving from previously screened to continually available plots, but not for those moving from continually available to previously-screened areas.