Recognition and avoidance of contaminated flowers by foraging bumblebees (Bombus terrestris)

Bumblebee colonies are founded by a single-mated queen. Due to this life history trait, bumblebees are more susceptible to parasites and diseases than polyandrous and/or polygynous social insects. A greater resistance towards parasites is shown when the genetic variability within a colony is increased. The parasite resistance may be divided into different levels regarding the step of the parasite infection (e.g. parasite uptake, parasite intake, parasite's establishment in the nest, parasite transmission). We investigate the prophylactic behaviour of bumblebees. Bumblebees were observed during their foraging flights on two artificial flowers; one of these was contaminated by Crithidia bombi, a naturally occurring gut parasite of bumblebees (in a control experiment the non-specific pathogen Escherichia coli was used). For C. bombi, bumblebees were preferentially observed feeding on the non-contaminated flower. Whereas for E. coli, the number of visits between flowers was the same, bumblebees spent more time feeding on the non-contaminated flower. These results demonstrate the ability of bumblebees to recognise the contamination of food sources. In addition, bumblebees have a stronger preference for the non-contaminated flower when C. bombi is present in the other flower than with E. coli which might be explained as an adaptive behaviour of bumblebees towards this specific gut parasite. It seems that the more specific the parasite is, the more it reduces the reward of the flower.     

Trade-off between travel distance and prioritization of high-reward sites in traplining bumblebees

1.Animals exploiting renewable resource patches are faced with complex multi-location routing problems. In many species, individuals visit foraging patches in predictable sequences called traplines. However, whether and how they optimize their routes remains poorly understood.2.In this study, we demonstrate that traplining bumblebees (Bombus terrestris) make a trade-off between minimizing travel distance and prioritizing the most rewarding feeding locations.3.Individual bees trained to forage on five artificial flowers of equal reward value selected the shortest possible route as a trapline. After introducing a single highly rewarding flower to the array, they re-adjusted their routes visiting the most rewarding flower first provided the departure distance from the shortest possible route remained small (18%). When routes optimizing the initial rate of reward intake were much longer (42%), bees prioritized short travel distances.4.Under natural conditions, in which individual flowers vary in nectar productivity and replenish continuously, it might pay bees to prioritize highly rewarding locations, both to minimize the overall number of flowers to visit and to beat competitors.5.We discuss how combined memories of location and quality of resource patches could allow bees and other traplining animals to optimize their routing decisions in heterogeneous environments.     

Nectar robbing improves male reproductive success of the endangered Aconitum napellus ssp. lusitanicum

Nectar robbery is usually thought to impact negatively on the reproductive success of plants, but also neutral or even positive effects have been reported. Very few studies have investigated the effects of nectar robbing on the behaviour of legitimate pollinators so far. Such behavioural changes may lead to the reduction of geitonogamy or to increased pollen movement. We simulated nectar robbing in experimental sites as well as in natural populations of Aconitum napellus ssp. lusitanicum, a rare plant pollinated by long-tongued bumblebees. In an experimental setup, we removed the nectaries of 40 % of the flowers, which is similar to rates of robbing observed in wild populations. Patches of plants with experimentally robbed flowers were compared with control patches containing plants with untreated flowers. We observed pollinator behaviour, mimicked male reproductive success (pollen dispersal) using fluorescent dye, and measured female reproductive success (seed set). The main legitimate visitors were bumblebees while honeybees were often observed robbing nectar. They did so by “base working”, i.e. sliding between tepals. Bumblebees tended to visit fewer flowers per plant and spent less time per single flower when these had been experimentally robbed. This change in behaviour consequently increased the proportion of flowers visited by bumblebees in patches with robbed flowers. Fluorescent dye mimicking pollen flow was dispersed larger distances after pollinators had visited patches with robbed flowers compared to control patches. Average seed set per plant was not affected by nectar robbing. Our results demonstrated that A. napellus does not suffer from nectar robbery but may rather benefit via improved pollen dispersal and thus, male reproductive success. Knowledge on such combined effects of behavioural changes of pollinators due to nectar robbery is important to understand the evolutionary significance of exploiters of such mutualistic relationships between plants and their pollinators.     

Foraging habitats and foraging distances of bumblebees, Bombus spp. (Hym., Apidae), in an agricultural landscape

Abstract: In selected foraging habitats of an agricultural landscape flower visits of bumblebees and community structure of foraging bumblebees were studied, with special regard to the role of crops as super-abundant resources. Most crops represent temporal foraging habitats with high abundance of bumblebees but mainly with low diversity in the bumblebee forage community, in contrast to permanent foraging habitats such as, for example, a hedgerow. The high numbers of bumblebees in the monoculture of crop plantations consisted mainly of short-tongued bumblebee species. The role of foraging distances for the visitation rate of foraging habitats was studied by performing capture–recapture experiments with natural nests of Bombus terrestris , Bombus lapidarius and Bombus muscorum . Differences were found on the species as well as the individual level. The foraging distances of B. muscorum were more restricted to the neighbourhood of the nesting habitat than the foraging activity of B. terrestris and B. lapidarius . High percentages of B. terrestris workers were recaptured while foraging on super-abundant resources in distances up to 1750 m from the nest. Isolated patches of highly rewarding forage crops, in agricultural landscapes, are probably only accessed by bumblebee species with large mean foraging distances, such as the short-tongued B. terrestris . Species like the rare, long-tongued B. muscorum depend on a close connection between nesting and foraging habitat. A restricted foraging radius might be one important factor of bumblebee species loss and potential pollinator limitation in modern agricultural landscapes. Furthermore, long-distance flights of bumblebee pollinators have to be considered in the present discussion on gene flow from transgenic plant species on a landscape scale.     

Travel optimization by foraging bumblebees through readjustments of traplines after discovery of new feeding locations

Animals collecting resources that replenish over time often visit patches in predictable sequences called traplines. Despite the widespread nature of this strategy, we still know little about how spatial memory develops and guides individuals toward suitable routes. Here, we investigate whether flower visitation sequences by bumblebees Bombus terrestris simply reflect the order in which flowers were discovered or whether they result from more complex navigational strategies enabling bees to optimize their foraging routes. We analyzed bee flight movements in an array of four artificial flowers maximizing interfloral distances. Starting from a single patch, we sequentially added three new patches so that if bees visited them in the order in which they originally encountered flowers, they would follow a long (suboptimal) route. Bees' tendency to visit patches in their discovery order decreased with experience. Instead, they optimized their flight distances by rearranging flower visitation sequences. This resulted in the development of a primary route (trapline) and two or three less frequently used secondary routes. Bees consistently used these routes after overnight breaks while occasionally exploring novel possibilities. We discuss how maintaining some level of route flexibility could allow traplining animals to cope with dynamic routing problems, analogous to the well-known traveling salesman problem.     

Genetic analysis of spatial foraging patterns and resource sharing in bumble bee pollinators

Conservation biologists, evolutionary ecologists and agricultural biologists require an improved understanding of how pollinators utilize space and share resources. Using microsatellite markers, we conducted a genetic analysis of space use and resource sharing at several spatial scales among workers of two ecologically dissimilar bumble bee species (Bombus terrestris and B. pascuorum) foraging in an urban landscape (London, UK). At fine scales, the relatedness of workers visiting small patches of flowers did not differ significantly from zero. Therefore, colonies shared flower patches randomly with other colonies, suggesting that worker scent-marks deterring visits to unrewarding flowers have not evolved as signals benefiting nestmates. To investigate space use at intermediate scales, we developed a program based on Thomas & Hill's maximum likelihood sibship reconstruction method to estimate the number of colonies utilizing single sites. The average number of colonies (95% confidence limits) sending workers to forage at sites of approximately 1 ha in area was 96 colonies (84-118) in B. terrestris and 66 colonies (61-76) in B. pascuorum. These values are surprisingly high and suggested that workers travelled far from their colonies to visit the sites. At the landscape scale, there was little or no genetic differentiation between sites. We conclude that urban habitats support large bumble bee populations and are potentially valuable in terms of bumble bee conservation. In addition, bumble bee-mediated gene flow in plants is likely to occur over large distances and plant-bumble bee conservation requires landscape-scale action.     

Floral colour change in Pedicularis monbeigiana (Orobanchaceae)

We examined the effects of the retention of colour-changed flowers on long- and short-distance attractiveness of bumblebees and the likelihood of successive flower visits by bumblebees in Pedicularis monbeigiana. The lower lip changed colour with age from white to purple. Hand geitonogamous pollination significantly reduced seed production. No pollen limitation occurred in this species. Purple-phase flowers contributed minimally to pollinator attractiveness at long distance. The combination of less reproductive flowers with a lower amount of reward and floral colour change enabled plants to direct pollinators to reproductive, highly rewarding white flowers at close range. A high percentage of purple-phase flowers in an inflorescence was associated with a marked reduction in the frequency of successive flower visits to individual plants. We suggest floral colour change in P. monbeigiana may serve as a mechanism for enhancing inter-individual pollen transfer and reducing intra-individual pollen transfer.     

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.     

Density-dependent and frequency-dependent selection by bumblebees Bombus terrestris (L.) (Hymenoptera: Apidae)

The behaviour of bumblebee workers foraging on arrays of artificial flowers of two colour morphs was observed. Experiments were conducted on arrays of varying morph frequencies and at three different total flower densities. Bumblebees consistently showed a preference for the commonest colour morph, and this behaviour was not significantly affected by changing density. In contrast, frequency-independent preferences changed significantly with density. At low densities, there was a strong bias towards the more conspicuous colour, whereas at higher densities there was no overall colour bias. Flight distances between flowers decreased significantly at high density. Bumblebees also visited flowers of similar colours sequentially, but this behaviour was not density-dependent. It is suggested that as densities increase, there is an increased probability that bumblebees detect yellow flowers, which were probably less conspicuous compared with blue flowers, and that this might be caused by changes in flight speed with flight distance. Where there is a positive relationship between pollinator visitation and the relative fitness of a floral morph, the observed behaviour would induce positive frequency-dependent selection on a plant population with two corolla colour morphs on which the bumblebees were foraging, which would result in stabilizing selection for a single corolla colour, irrespective of density. There was no indication that rare colour morphs would be preferred at high density. The probability of different corolla colour morphs going to fixation would, however, be affected by density.     

Bumblebee visits to Impatiens spp.: pattern and efficiency

Summary Three Japanese species of Impatiens, which secrete nectar continuously in long spurs, were visited by Bombus diversus workers consecutively throughout the day. B. diversus workers showed characteristic patterns of behavior in flower use, flower choice, and patch departure. (1) Bumblebees stayed longer on a flower which had been unvisited for a while than on a flower which had been visited recently. (2) Bumblebees preferred visiting flowers which had been unvisited for a while to visiting those which had been visited recently, and to visiting those which had been unvisited for a long period. (3) Bumblebees had a higher probability of leaving a patch after they had stayed on a flower for a short period than after they had stayed for a longer period. The bumblebees appeared to perceive both remotely and proximately chemical cues deposited by other foraging individuals, which indicated nectar rewards in a flower, and thus obtained a higher nectar intake than the mean amount of nectar left in a flower.     

Optimal foraging in bumblebees and coevolution with their plants

Summary The aims of this paper were to consider the coevolution between bumblebee movement patterns within plants and various properties of the plants such as the spatial distribution of their flowers, and to determine the extent to which the bumblebees and the plants can be considered to be maximally adaptive or optimal. Attention was restricted to plants which have flowers arranged on vertical inflorescences and to the bumblebees which visit these plants.It was found that the bumblebees tend to commence foraging at the bottom of each infloresence, that they tend to move from one flower to the closest vertically higher flower, that they miss flowers as they move upwards and that they tend to leave each inflorescence before reaching the top. It was also found for the four common plant species considered that nectar abundance per flower decreases with flower height on an inflorescence, that the flowers with receptive stigmas are restricted to the bottoms of the inflorescences while the flowers shedding pollen occur above them, and that the flowers are arranged approximately in spirals on the inflorescences.The pattern of movements of the bumblebees and the various properties of the plants appear to represent coevolved adaptations. Furthermore the bumblebees' movement patterns appear to be optimal in the sense that they result in the maximum net rate of energy gain to the bumblebees. Further studies are necessary, however, to determine whether or not the plants can be considered to be optimal.An exception to the above scheme is provided by a plant which is quite uncommon in the study area. This plant also has flowers on vertical inflorescences and appears to be pollinated by bumblebees. However, while the pattern of movements of the bumblebees on this plant species are extremely similar to those on the four common species, this plant species exhibits quite different properties from the other four. Two possible explanations for this exception are presented.     

Foraging strategies of insects for gathering nectar and pollen, and implications for plant ecology and evolution

The majority of species of flowering plants rely on pollination by insects, so that their reproductive success and in part their population structure are determined by insect behaviour. The foraging behaviour of insect pollinators is flexible and complex, because efficient collection of nectar or pollen is no simple matter. Each flower provides a variable but generally small reward that is often hidden, flowers are patchily distributed in time and space, and are erratically depleted of rewards by other foragers. Insects that specialise in visiting flowers have evolved an array of foraging strategies that act to improve their efficiency, which in turn determine the reproductive success of the plants that they visit. This review attempts a synthesis of the recent literature on selectivity in pollinator foraging behaviour, in terms of the species, patch and individual flowers that they choose to visit.

The variable nature of floral resources necessitate foraging behaviour based upon flexible learning, so that foragers can respond to the pattern of rewards that they encounter. Fidelity to particular species allows foragers to learn appropriate handling skills and so reduce handling times, but may also be favoured by use of a search image to detect flowers. The rewards received are also used to determine the spatial patterns of searches; distance and direction of flights are adjusted so that foragers tend to remain within rewarding patches and depart swiftly from unrewarding ones. The distribution of foragers among patchy resources generally conforms to the expectations of two simple optimal foraging models, the ideal free distribution and the marginal value theorem.

Insects are able to learn to discriminate among flowers of their preferred species on the basis of subtle differences in floral morphology. They may discriminate upon the basis of flower size, age, sex or symmetry and so choose the more rewarding flowers. Some insects are also able to distinguish and reject depleted flowers on the basis of ephemeral odours left by previous visitors. These odours have recently been implicated as a mechanism involved in interspecific interactions between foragers.

From the point of view of a plant reliant upon insect pollination, the behaviour of its pollinators (and hence its reproductive success) is likely to vary according to the rewards offered, the size and complexity of floral displays used to advertise their location, the distribution of conspecific and of rewards offered by other plant species, and the abundance and behaviour of other flower visitors.     

Pollinator community responses to the spatial population structure of wild plants: A pan-European approach

Land-use changes can alter the spatial population structure of plant species, which may in turn affect the attractiveness of flower aggregations to different groups of pollinators at different spatial scales. To assess how pollinators respond to spatial heterogeneity of plant distributions and whether honeybees affect visitation by other pollinators we used an extensive data set comprising ten plant species and their flower visitors from five European countries. In particular we tested the hypothesis that the composition of the flower visitor community in terms of visitation frequencies by different pollinator groups were affected by the spatial plant population structure, viz. area and density measures, at a within-population (‘patch’) and among-population (‘population’) scale. We found that patch area and population density were the spatial variables that best explained the variation in visitation frequencies within the pollinator community. Honeybees had higher visitation frequencies in larger patches, while bumblebees and hoverflies had higher visitation frequencies in sparser populations. Solitary bees had higher visitation frequencies in sparser populations and smaller patches. We also tested the hypothesis that honeybees affect the composition of the pollinator community by altering the visitation frequencies of other groups of pollinators. There was a positive relationship between visitation frequencies of honeybees and bumblebees, while the relationship with hoverflies and solitary bees varied (positive, negative and no relationship) depending on the plant species under study. The overall conclusion is that the spatial structure of plant populations affects different groups of pollinators in contrasting ways at both the local (‘patch’) and the larger (‘population’) scales and, that honeybees affect the flower visitation by other pollinator groups in various ways, depending on the plant species under study. These contrasting responses emphasize the need to investigate the entire pollinator community when the effects of landscape change on plant–pollinator interactions are studied.     

Ineffectiveness of nectar scent in generating bumblebee visits to flowers of Impatiens textori

To clarify if bumblebees can recognize nectar through its scent in Impatiens textori flowers, we examined the behavior of Bombus diversus on nectarless flowers in which the spurs had been artificially removed. Bumblebee visits to both natural flowers and spur‐cut flowers were captured using a long‐term video recording system. Visiting behavior and frequency were compared between the two flower types. Many bumblebees visited both types of flower, and their visit frequencies were not significantly different. However, the length of stay on each flower type did differ, with the bumblebees remaining on the spur‐cut flowers for a significantly shorter time than on the natural flowers. Our results suggest that bumblebees cannot detect the absence of nectar in I. textori flowers before probing them. Therefore, the nectar scent of I. textori does not serve to attract bumblebees although the presence of nectar will detain bumblebees on flowers for longer periods.     

Pollinator visitation to mass-flowering courgette and co-flowering wild flowers: Implications for pollination and bee conservation on farms

Managing the complex relationship between pollinators and their habitat requirements is of particular concern to growers of pollinator-dependent crop species, such as courgette (Cucurbita pepo). Naturally occurring wild flowers (i.e. agricultural weeds) offer a free, sustainable, and often underappreciated resource for pollinators, however, they may compete with crop flowers for visits. To understand the extent to which floral resources mediate pollinator visitation to courgette flowers and courgette fields, plant community and pollinator visitation data were collected at two spatial scales: field scale (in margins, and in the cropped area) and farm scale (500 m and 2000 m radii) for nine courgette fields across the UK. Apis mellifera (honeybees) and Bombus spp. (bumblebees) were the only pollinators observed to visit courgette flowers. Bumblebees were significantly more abundant on courgette flowers in fields with a greater species richness of wild flowers in the crop, whilst honeybees were significantly more abundant on courgette flowers in areas with less semi-natural habitat. For both honeybees and bumblebees, their abundance in field margins did not significantly reduce their abundance on courgette flowers, suggesting that wild flowers were not competing with courgette flowers for pollinator visitation. Although solitary bees were not observed to visit courgette flowers, their abundance and species richness in courgette fields were significantly greater with more semi-natural habitat and a greater species richness of wild flowers. Therefore, allowing uncultivated areas around the crop to be colonised by species-rich wild flowers is an effective way of boosting the abundance of bumblebees, which are important visitors to courgette flowers, as well as the abundance and species richness of solitary bees, thereby benefitting pollinator conservation.     

草乌花蜜产量的梯度分布及熊蜂自下而上的访花行为

收益降低假说(declining reward hypothesis)认为熊蜂自下而上的访花顺序是对花蜜产量的直接响应,先访问下部花蜜产量高的花可以获得更多的收益;花开口方向假说认为自下而上访花是因为熊蜂更容易看见其上部的花朵。为了验证上述两个假说,我们于2008年8月在北京小龙门国家森林公园调查了红光熊蜂(Bombus ignitus)访问草乌(Aconitum kusnezoffii)直立和倒立顶生花序的访问顺序,测量了直立花序下部雌性阶段花和上部雄性阶段花花蜜的糖浓度、体积,计算了花蜜中的糖含量。结果表明,红光熊蜂在直立花序和倒立花序内均以向上运动为主,分别占总运动次数的62.77%和68.35%;直立花序下部雌性阶段花花蜜糖浓度比上部雄性阶段花低1.44%,但是花蜜体积和花蜜中的糖含量都显著高于雄性阶段的花。由于熊蜂访问倒立花序时先访问的是下部的低回报雄性阶段的花,然后再访问上部高回报的雌性阶段的花,这与收益降低假说矛盾,表明红光熊蜂自下而上访问草乌直立花序可能不是受到花蜜产量的调节。     

The effect of proboscis and corolla tube lengths on patterns and rates of flower visitation by bumblebees

Summary The rates at which bumblebees of different proboscis lengths forage on flowers of a series of corolla tube lengths were determined. The results indicate significant correlations between proboscis length and time spent by bees on flowers. Bumblebees of long proboscis length can forage significantly faster than bees of shorter proboscis length on flowers with long corolla tubes. There is also evidence which suggests that bumblebees of short proboscis length prefer and are more efficient on short corolla tubes. These results support the use of proboscis length as a morphological indicator of resource utilization in bumblebees.     

Flight patterns of foraging bees relative to density of artificial flowers and distribution of nectar

Summary Flight patterns of honeybees (Apis mellifera ligustica) were quantified as the bees foraged among artificial flowers for sugar solution (nectar). Bees exhibited considerable directionality on successive flights which minimized repeat visits to flowers and they usually made short flights to nearby flowers, thus minimizing flight time. The change in direction on successive flights between flowers were independent of the number of immediately preceding consecutive rewarding visits but decreased as the number of non-rewarding visits increased. Flight distances were short after visits to rewarding flowers but increased as the number of immediately preceding non-rewarding visits increased. The bees' rate of caloric intake (calories/time) was highest at the floral arrays having the highest density, and it was greater at arrays with clumped nectar-distributions than at those with randomly distributed nectar. These findings are explained in terms of the observed flight patterns.Contribution number 1660 from the Department of Entomology, University of Kansas, Lawrence, Kansas 66045, USA     

Size-dependent pollination efficiency in Anchusa officinalis (Boraginaceae): causes and consequences

Summary Bumblebees foraging on the self-incompatible Anchusa officinalis fly between near neighbour plants and between near neighbour inflorescences within plants. Although many-flowered plants attracted most bumblebees these plants received fewer visits on a per flower basis than smaller plants, and each bumblebee visited a smaller proportion of the flowers. The calculated effective visitation rate per flower was highest on plants of an intermediate size. If pollen-carryover was assumed to be limited the most efficient plant was predicted to be smaller since the proportion of fertilized flowers per bumblebee visit is expected to decrease further on the largest plants in relation to the total flower number. These predictions were tested by measuring fruit-set in the field. The percentage fruit-set decreased with plant size at all sizes that were investigated. That the most efficient plant was small indicates that pollen-carryover was indeed limited. However, the low percentage fruit-set associated with large size did not present a serious problem since the total estimated seed production per plant still increased with size. Selection favoring smaller plants may be low or absent in Anchusa.     

Radar Tracking and Motion-Sensitive Cameras on Flowers Reveal the Development of Pollinator Multi-Destination Routes over Large Spatial Scales

Central place foragers, such as pollinating bees, typically develop circuits (traplines) to visit multiple foraging sites in a manner that minimizes overall travel distance. Despite being taxonomically widespread, these routing behaviours remain poorly understood due to the difficulty of tracking the foraging history of animals in the wild. Here we examine how bumblebees (Bombus terrestris) develop and optimise traplines over large spatial scales by setting up an array of five artificial flowers arranged in a regular pentagon (50 m side length) and fitted with motion-sensitive video cameras to determine the sequence of visitation. Stable traplines that linked together all the flowers in an optimal sequence were typically established after a bee made 26 foraging bouts, during which time only about 20 of the 120 possible routes were tried. Radar tracking of selected flights revealed a dramatic decrease by 80% (ca. 1500 m) of the total travel distance between the first and the last foraging bout. When a flower was removed and replaced by a more distant one, bees engaged in localised search flights, a strategy that can facilitate the discovery of a new flower and its integration into a novel optimal trapline. Based on these observations, we developed and tested an iterative improvement heuristic to capture how bees could learn and refine their routes each time a shorter route is found. Our findings suggest that complex dynamic routing problems can be solved by small-brained animals using simple learning heuristics, without the need for a cognitive map.