Foraging scent marks of bumblebees: footprint cues rather than pheromone signals

In their natural habitat foraging bumblebees refuse to land on and probe flowers that have been recently visited (and depleted) by themselves, conspecifics or other bees, which increases their overall rate of nectar intake. This avoidance is often based on recognition of scent marks deposited by previous visitors. While the term 'scent mark' implies active labelling, it is an open question whether the repellent chemicals are pheromones actively and specifically released during flower visits, or mere footprints deposited unspecifically wherever bees walk. To distinguish between the two possibilities, we presented worker bumblebees (Bombus terrestris) with three types of feeders in a laboratory experiment: unvisited control feeders, passive feeders with a corolla that the bee had walked over on its way from the nest (with unspecific footprints), and active feeders, which the bee had just visited and depleted, but which were immediately refilled with sugar-water (potentially with specific scent marks). Bumblebees rejected both active and passive feeders more frequently than unvisited controls. The rate of rejection of passive feeders was only slightly lower than that of active feeders, and this difference vanished completely when passive corollas were walked over repeatedly on the way from the nest. Thus, mere footprints were sufficient to emulate the repellent effect of an actual feeder visit. In confirmation, glass slides on which bumblebees had walked on near the nest entrance accumulated hydrocarbons (alkanes and alkenes, C23 to C31), which had previously been shown to elicit repellency in flower choice experiments. We conclude that repellent scent marks are mere footprints, which foraging bees avoid when they encounter them in a foraging context.     

Floral colour change in <Emphasis Type="Italic">Byrsonima variabilis</Emphasis> (Malpighiaceae) as a visual cue for pollen but not oil foraging by oil-collecting bees

Pollinators search for multiple flora resources throughout their life cycle. Most studies, however, only assess how bees discriminate floral cues in the context of nectar foraging. In the present study, we sought to elucidate whether oil-collecting bees discriminate flowers of Byrsonima variabilis (Malpighiaceae) with petals of different colours when foraging for pollen or oil. As the colour of the standard petal changes during anthesis, we characterised the spectral reflectance patterns of flowers throughout anthesis and modelled chromatic perceptual space to determine how these colour patterns are perceived by bees. Through the quantification of flower pollen in the different phases, we found that the colour of the standard petal is an honest cue of the presence of pollen. Centridine bees preferentially visited flowers with a yellow (bee’s green) colour when searching for pollen, but indiscriminately visited flowers with different petal colours when searching for floral oil. We suggest that standard petals, in the species studied and others of the genus, like nectar guides, act as pollen guides, which oil-collecting females use to detect pollen-rich flowers. Moreover, they use different floral clues during foraging for different resources in the same host plant.     

Flower-visiting behavior of male bees is triggered by nectar-feeding insects

Bees are important pollinators for many flowering plants. Female bees are thought to be more effective pollinators than male bees because they carry much more pollen than males. Males of some solitary bee species are known to patrol near flowers that females visit. Because patrolling males visit flowers to mate or defend their territories, they may function as pollinators. However, the significance of patrolling males to pollination has not been studied. We studied males of a solitary bee, Heriades fulvohispidus (Megachilidae), patrolling near flowers and visiting flowers that attracted nectar-feeding insects, including conspecifics, on the Ogasawara (Bonin) Islands. To test the hypothesis that patrolling male bees may function as pollen vectors, we compared the frequency of visits by H. fulvohispidus to flowers of an endemic plant, Schima mertensiana (Theaceae); comparisons were made among flowers with a dead H. fulvohispidus, a dead beetle, a piece of plastic, and nothing (control flowers). Patrolling H. fulvohispidus more frequently visited flowers with a dead conspecific, a dead beetle, or a piece of plastic than the control flowers. Our experiment demonstrates that nectar-feeding insects (including conspecifics and other insects) enhance the flower-visiting frequency of patrolling H. fulvohispidus males on S. mertensiana flowers. Furthermore, we observed S. mertensiana pollen on patrolling males as well as females, suggesting that male bees may also function as pollen vectors.     

Nectar production dynamics and sugar composition in two <Emphasis Type="Italic">Mucuna</Emphasis> species (Leguminosae,Faboideae) with different specialized pollinators

Nectar is secreted in particular rhythms throughout the lifespan of a flower, which allows determining the nectar production dynamics. This paper compares nectar features in Mucuna japira and Mucuna urens describing: dynamics of nectar production, floral response to nectar removal, resorption, nectar sugar composition, and variation in nectar sugar composition. M. japira inflorescence bears 12–21 yellow flowers, which are in anthesis for 7 days, whereas M. urens inflorescence bears 36–54 greenish flowers, but only 1–3 flowers are in anthesis simultaneously that last one night. Nectar volume and sugar concentration were measured, and the amount of sugar was estimated. Qualitative and quantitative nectar sugar composition was determined. Both species had a constant nectar sugar concentration (ca. 10% for M. japira and ca. 16% for M. urens) and secreted high volumes of nectar (ca. 340 μl per flower for M. japira and 310 μl per flower for M. urens), during 5 days for M. japira and 6 h for M. urens, but after the first removal, i.e., when flower opening mechanism is triggered, nectar production stops immediately. Nectar resorption occurred in both species. Nectar sugar composition showed some similarities between the species. Variation in nectar sugar composition occurred in both species. The Mucuna species are dependent on their pollinators to produce fruits and seeds, and they have different strategies to promote the necessary interaction with birds or bats, especially related to nectar and flower characteristics.     

Conspecific flowers of <Emphasis Type="Italic">Sinapis arvensis</Emphasis> are stronger competitors for pollinators than those of the invasive weed <Emphasis Type="Italic">Bunias orientalis</Emphasis>

Biological invasions can affect the structure and function of ecosystems and threaten native plant species. Since most weeds rely on mutualistic relationships in their new environment, they may act as new competitors for pollinators. Pollinator competition is likely to be density dependent, but it is often difficult to disentangle competition caused by flower quality from effects caused by flower quantity. In order to test the effects of the presence and number of flowers of the invasive weed Bunias orientalis on the insect visitation rates in a native species (Sinapis arvensis), we performed two replacement experiments using plants with standardised flower numbers. The visitation rates in S. arvensis were significantly higher than in B. orientalis and the number of insect visits dropped significantly with increasing density of S. arvensis flowers. These results suggest that intraspecific competition among flowers of S. arvensis is stronger than the competitive effect of alien flowers. As flowers of B. orientalis do not seem to distract visitors from S. arvensis, it is unlikely that pollinator competition between these two plant species plays a crucial role. However, it cannot be excluded that mass blossom stands of B. orientalis may distract flower visitors from native species.     

Indirect interactions between invasive and native plants via pollinators

In generalised pollination systems, the presence of alien plant species may change the foraging behaviour of pollinators on native plant species, which could result in reduced reproductive success of native plant species. We tested this idea of indirect interactions on a small spatial and temporal scale in a field study in Mauritius, where the invasive strawberry guava, Psidium cattleianum, provides additional floral resources for insect pollinators. We predicted that the presence of flowering guava would indirectly and negatively affect the reproductive success of the endemic plant Bertiera zaluzania, which has similar flowers, by diverting shared pollinators. We removed P. cattleianum flowers within a 5-m radius from around half the B. zaluzania target plants (treatment) and left P. cattleianum flowers intact around the other half (control). By far, the most abundant and shared pollinator was the introduced honey bee, Apis mellifera, but its visitation rates to treatment and control plants were similar. Likewise, fruit and seed set and fruit size and weight of B. zaluzania were not influenced by the presence of P. cattleianum flowers. Although other studies have shown small-scale effects of alien plant species on neighbouring natives, we found no evidence for such negative indirect interactions in our system. The dominance of introduced, established A. mellifera indicates their replacement of native insect flower visitors and their function as pollinators of native plant species. However, the pollination effectiveness of A. mellifera in comparison to native pollinators is unknown. Christine B. Müller, deceased 7 March 2008.     

Floral CO<Subscript>2</Subscript> emission may indicate food abundance to nectar-feeding moths

As part of a study of the roles of the sensory subsystem devoted to CO₂ in the nectar-feeding moth Manduca sexta, we investigated CO₂ release and nectar secretion by flowers of Datura wrightii, a preferred hostplant of Manduca. Datura flowers open at dusk and wilt by the following noon. During the first hours after dusk, when Manduca feeds, the flowers produce considerable amounts of nectar and emit levels of CO₂ that should be detectable by moths nearby. By midnight, however, both nectar secretion and CO₂ release decrease significantly. Because nectar production requires high metabolic activity, high floral CO₂ emission may indicate food abundance to the moths. We suggest that hovering moths could use the florally emitted CO₂ to help them assess the nectar content before attempting to feed in order to improve their foraging efficiency.Electronic Supplementary Material  Supplementary material is available in the online version of this article at     

The innate responses of bumble bees to flower patterns: separating the nectar guide from the nectary changes bee movements and search time

Nectar guides can enhance pollinator efficiency and plant fitness by allowing pollinators to more rapidly find and remember the location of floral nectar. We tested if a radiating nectar guide around a nectary would enhance the ability of naïve bumble bee foragers to find nectar. Most experiments that test nectar guide efficacy, specifically radiating linear guides, have used guides positioned around the center of a radially symmetric flower, where nectaries are often found. However, the flower center may be intrinsically attractive. We therefore used an off-center guide and nectary and compared “conjunct” feeders with a nectar guide surrounding the nectary to “disjunct” feeders with a nectar guide separated from the nectary. We focused on the innate response of novice bee foragers that had never previously visited such feeders. We hypothesized that a disjunct nectar guide would conflict with the visual information provided by the nectary and negatively affect foraging. Approximately, equal numbers of bumble bees (Bombus impatiens) found nectar on both feeder types. On disjunct feeders, however, unsuccessful foragers spent significantly more time (on average 1.6-fold longer) searching for nectar than any other forager group. Successful foragers on disjunct feeders approached these feeders from random directions unlike successful foragers on conjunct feeders, which preferentially approached the combined nectary and nectar guide. Thus, the nectary and a surrounding nectar guide can be considered a combination of two signals that attract naïve foragers even when not in the floral center.     

Pollen foraging: learning a complex motor skill by bumblebees (<Emphasis Type="Italic">Bombus terrestris</Emphasis>)

To investigate how bumblebees (Bombus terrestris) learn the complex motor skills involved in pollen foraging, we observed naïve workers foraging on arrays of nectarless poppy flowers (Papaver rhoeas) in a greenhouse. Foraging skills were quantified by measuring the pollen load collected during each foraging bout and relating this to the number of flowers visited and bout duration on two consecutive days. The pollen standing crop (PSC) in each flower decreased drastically from 0530 to 0900 hours. Therefore, we related foraging performance to the changing levels of pollen available (per flower) and found that collection rate increased over the course of four consecutive foraging bouts (comprising between 277 and 354 individual flower visits), suggesting that learning to forage for pollen represents a substantial time investment for individual foragers. The pollen collection rate and size of pollen loads collected at the start of day 2 were markedly lower than at the end of day 1, suggesting that components of pollen foraging behaviour could be subject to imperfect overnight retention. Our results suggest that learning the necessary motor skills to collect pollen effectively from morphologically simple flowers takes three times as many visits as learning how to handle the most morphologically complex flowers to extract nectar, potentially explaining why bees are more specialised in their choice of pollen flowers.     

Sticky snack for sengis: The Cape rock elephant-shrew, Elephantulus edwardii (Macroscelidea), as a pollinator of the Pagoda lily, Whiteheadia bifolia (Hyacinthaceae)

Following the recent discovery of rodent pollination in the Pagoda lily, Whiteheadia bifolia (Hyacinthaceae) in South Africa, now the Cape rock elephant-shrew, Elephantulus edwardii (Macroscelidea, Afrotheria) is reported as an additional pollinator. Elephant-shrews, live-trapped near W. bifolia plants, were released in two terraria, containing the plants. The animals licked nectar with their long and slender tongues while being dusted with pollen and touching the stigmas of the flowers with their long and flexible noses. The captured elephant-shrews had W. bifolia pollen in their faeces, likely as a result of grooming their fur as they visited the flowers without eating or destroying them. The animals mostly preferred nectar over other food. This is the first record of pollination and nectar consumption in the primarily insectivorous E. edwardii, contributing to the very sparse knowledge about the behaviour of this unique clade of African mammals, as well as pollination by small mammals.     

Bird pollination of Canary Island endemic plants

The Canary Islands are home to a guild of endemic, threatened bird-pollinated plants. Previous work has suggested that these plants evolved floral traits as adaptations to pollination by flower specialist sunbirds, but subsequently, they appear to have co-opted generalist passerine birds as sub-optimal pollinators. To test this idea, we carried out a quantitative study of the pollination biology of three of the bird-pollinated plants, Canarina canariensis (Campanulaceae), Isoplexis canariensis (Veronicaceae) and Lotus berthelotii (Fabaceae), on the island of Tenerife. Using colour vision models, we predicted the detectability of flowers to bird and bee pollinators. We measured pollinator visitation rates, nectar standing crops as well as seed-set and pollen removal and deposition. These data showed that the plants are effectively pollinated by non-flower specialist passerine birds that only occasionally visit flowers. The large nectar standing crops and extended flower longevities (>10 days) of Canarina and Isoplexis suggests that they have evolved a bird pollination system that effectively exploits these low frequency non-specialist pollen vectors and is in no way sub-optimal. Seed set in two of the three species was high and was significantly reduced or zero in flowers where pollinator access was restricted. In L. berthelotii, however, no fruit set was observed, probably because the plants were self-incompatible horticultural clones of a single genet. We also show that, while all three species are easily detectable for birds, the orange Canarina and the red Lotus (but less so the yellow-orange Isoplexis) should be difficult to detect for insect pollinators without specialised red receptors, such as bumblebees. Contrary to expectations if we accept that the flowers are primarily adapted to sunbird pollination, the chiffchaff (Phylloscopus canariensis) was an effective pollinator of these species.     

The influence of pigmentation patterning on bumblebee foraging from flowers of Antirrhinum majus

Patterns of pigmentation overlying the petal vasculature are common in flowering plants and have been postulated to play a role in pollinator attraction. Previous studies report that such venation patterning is significantly more attractive to bee foragers in the field than ivory or white flowers without veins. To dissect the ways in which venation patterning of pigment can influence bumblebee behaviour, we investigated the response of flower-naïve individuals of Bombus terrestris to veined, ivory and red near-isogenic lines of Antirrhinum majus. We find that red venation shifts flower colour slightly, although the ivory background is the dominant colour. Bees were readily able to discriminate between ivory and veined flowers under differential conditioning but showed no innate preference when presented with a free choice of rewarding ivory and veined flowers. In contrast, both ivory and veined flowers were selected significantly more often than were red flowers. We conclude that advantages conferred by venation patterning might stem from bees learning of their use as nectar guides, rather than from any innate preference for striped flowers.     

Longer visits on familiar plants?: testing a regular visitor’s tendency to probe more flowers than occasional visitors

An individual pollinator may tend to consecutively probe more flowers on a plant to which it returns at shorter intervals than other plants. In a large net cage, I let individually marked bumble bees forage on flowering heads of red clovers arranged in 37 bottles (plants), each of which was monitored by an observer to record every visit and probe for 2.5 h on each of 3 days. The data of collective visits by marked individuals revealed that the bees had their own foraging areas, in which they visited a set of plants frequently and others less often, i.e., the same individual bee repeatedly returned to certain plants as a regular visitor while sampling others as an occasional visitor. I further found that as a regular visitor, an individual bee tended to probe more flowering heads on familiar plants while probing fewer on unfamiliar plants as an occasional visitor. The mean number of consecutive probes by a bee was also positively correlated with its activity (the total number of plant visits made during the observation period). The fact that each bee behaves differently on different plants indicates that the same individual pollinator can exert different influence on the reproductive success of each plant: apparently, a pollinator likely reduces the potential for geitonogamous self-pollination when foraging as an occasional visitor. Attracting occasional visitors therefore may be beneficial for plants to avoid geitonogamy. This study thus emphasizes the importance of paying attention to pollinator individuality in pollination ecology.     

Hesitation behaviour of hoverflies Sphaerophoria spp. to avoid ambush by crab spiders

Pollinators possess several antipredator adaptations that minimise predation risk during foraging. In addition to morphological adaptations, hoverflies might have behavioural antipredator adaptations. We conducted three field experiments to investigate whether the "hesitation behaviour" of hoverflies Sphaerophoria spp., moving backwards and forwards in front of a flower, is effective in avoiding ambush predators on flowers. First, we compared the behaviour of different flower visitors, including several bees and other hoverflies, with Sphaerophoria spp. behaviour. Only Sphaerophoria spp. exhibited the hesitation behaviour in front of flowers. The flight behaviour was observed more frequently before landing on flowers than on leaves. Second, we investigated rejection by Sphaerophoria spp. to artificially placed corpses of the crab spider Thomisus labefactus. The rejection rate of flowers with a crab spider placed on or under it was significantly higher than that of non-treated flowers. Moreover, the presence of a spider on the flower decreased the number of hesitation displays, compared with non-treated flowers. Finally, to determine whether hesitation behaviour could be a consequence of floral assessment, we investigated hoverfly rejection of previously foraged flowers. Sphaerophoria spp. did not reject flowers that had been visited by the same individual or conspecifics within 3 min. We suggest that hesitation behaviour may be adaptive, enabling assessment of predation risk and hence avoiding ambush predators on flowers.     

Direct and indirect fossil records of megachilid bees from the Paleogene of Central Europe (Hymenoptera: Megachilidae)

Aside from pollen and nectar, bees of the subfamily Megachilinae are closely associated with plants as a source of materials for nest construction. Megachilines use resins, masticated leaves, trichomes and other plant materials sometimes along with mud to construct nests in cavities or in soil. Among these, the leafcutter bees (Megachile s.l.) are the most famous for their behaviour to line their brood cells with discs cut from various plants. We report on fossil records of one body fossil of a new non-leafcutting megachiline and of 12 leafcuttings from three European sites—Eckfeld and Messel, both in Germany (Eocene), and Menat, France (Paleocene). The excisions include the currently earliest record of probable Megachile activity and suggest the presence of such bees in the Paleocene European fauna. Comparison with extant leafcuttings permits the interpretation of a minimal number of species that produced these excisions. The wide range of size for the leafcuttings indirectly might suggest at least two species of Megachile for the fauna of Messel in addition to the other megachiline bee described here. The presence of several cuttings on most leaves from Eckfeld implies that the preferential foraging behaviour of extant Megachile arose early in megachiline evolution. These results demonstrate that combined investigation of body and trace fossils complement each other in understanding past biodiversity, the latter permitting the detection of taxa not otherwise directly sampled and inferences on behavioural evolution.     

Pesticide exposure in honey bees results in increased levels of the gut pathogen <Emphasis Type="Italic">Nosema</Emphasis>

Global pollinator declines have been attributed to habitat destruction, pesticide use, and climate change or some combination of these factors, and managed honey bees, Apis mellifera, are part of worldwide pollinator declines. Here we exposed honey bee colonies during three brood generations to sub-lethal doses of a widely used pesticide, imidacloprid, and then subsequently challenged newly emerged bees with the gut parasite, Nosema spp. The pesticide dosages used were below levels demonstrated to cause effects on longevity or foraging in adult honey bees. Nosema infections increased significantly in the bees from pesticide-treated hives when compared to bees from control hives demonstrating an indirect effect of pesticides on pathogen growth in honey bees. We clearly demonstrate an increase in pathogen growth within individual bees reared in colonies exposed to one of the most widely used pesticides worldwide, imidacloprid, at below levels considered harmful to bees. The finding that individual bees with undetectable levels of the target pesticide, after being reared in a sub-lethal pesticide environment within the colony, had higher Nosema is significant. Interactions between pesticides and pathogens could be a major contributor to increased mortality of honey bee colonies, including colony collapse disorder, and other pollinator declines worldwide.     

Background complexity affects colour preference in bumblebees

Flowers adapted for hummingbird pollination are typically red. This correlation is usually explained by the assertion that nectar- or pollen-stealing bees are “blind” to red flowers. However, laboratory studies have shown that bees are capable of locating artificial red flowers and often show no innate preference for blue over red. We hypothesised that these findings might be artefacts of the simplified laboratory environment. Using bumblebees (Bombus impatiens) that had been trained to visit red and blue artificial flowers, we tested whether colour preference was influenced by complexity of the background on which they were foraging. Many bees were indifferent to flower colour when tested using a uniform green background like those commonly used in laboratory studies, but all bees showed strong colour preferences (usually for blue) when flowers were presented against a photograph of real foliage. Overall, preference for blue flowers was significantly greater on the more realistic, complex background. These results support the notion that the red of “hummingbird syndrome” flowers can function to reduce bee visits despite the ability of bees to detect red and highlight the need to consider context when drawing inferences about pollinator preferences from laboratory data. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Highly controlled nest homeostasis of honey bees helps deactivate phenolics in nectar

Honey bees have a highly developed nest homeostasis, for example, maintaining low CO₂ levels and stable nest temperatures at 35°C.We investigate the role of nest homeostasis in deactivating phenolic compounds present in the nectar of Aloe littoralis. We show that the phenolic content in nectar was reduced (from 0.65% to 0.49%) after nectar was incubated in a nest of Apis cerana, and that it was reduced still more (from 0.65% to 0.37%) if nectar was mixed with hypopharyngeal gland proteins (HGP) of worker bees before being placed inside a nest. HGP had little effect on samples outside a nest, indicating that nest conditions are necessary for HGP to deactivate phenolics in nectar. Consequently, the highly controlled nest homeostasis of honey bees facilitates direct deactivation of phenolics in nectar, and plays a role in the action of HGP as well.     

The cues have it; nest-based, cue-mediated recruitment to carbohydrate resources in a swarm-founding social wasp

This study explores whether or not foragers of the Neotropical swarm-founding wasp Polybia occidentalis use nest-based recruitment to direct colony mates to carbohydrate resources. Recruitment allows social insect colonies to rapidly exploit ephemeral resources, an ability especially advantageous to species such as P. occidentalis, which store nectar and prey in their nests. Although recruitment is often defined as being strictly signal mediated, it can also occur via cue-mediated information transfer. Previous studies indicated that P. occidentalis employs local enhancement, a type of cue-mediated recruitment in which the presence of conspecifics at a site attracts foragers. This recruitment is resource-based, and as such, is a blunt recruitment tool, which does not exclude non-colony mates. We therefore investigated whether P. occidentalis also employs a form of nest-based recruitment. A scented sucrose solution was applied directly to the nest. This mimicked a scented carbohydrate resource brought back by employed foragers, but, as foragers were not allowed to return to the nest with the resource, there was no possibility for on-nest recruitment behavior. Foragers were offered two dishes—one containing the test scent and the other an alternate scent. Foragers chose the test scent more often, signifying that its presence in the nest induces naïve foragers to search for it off-nest. P. occidentalis, therefore, employs a form of nest-based recruitment to carbohydrate resources that is mediated by a cue, the presence of a scented resource in the nest.     

Experience,but not distance,influences the recruitment precision in the stingless bee <Emphasis Type="Italic">Scaptotrigona mexicana</Emphasis>

Recruitment precision, i.e. the proportion of recruits that reach an advertised food source, is a crucial adaptation of social bees to their environment. Studies with honeybees showed that recruitment precision is not a fixed feature, but it may be enhanced by factors like experience and distance. However, little is known regarding the recruitment precision of stingless bees. Hence, in this study, we examined the effects of experience and spatial distance on the precision of the food communication system of the stingless bee Scaptotrigona mexicana. We conducted the experiments by training bees to a three-dimensional artificial patch at several distances from the colony. We recorded the choices of individual recruited foragers, either being newcomers (foragers without experience with the advertised food source) or experienced (foragers that had previously visited the feeder). We found that the average precision of newcomers (95.6 ± 2.61%) was significantly higher than that of experienced bees (80.2 ± 1.12%). While this might seem counter-intuitive on first sight, this “loss” of precision can be explained by the tendency of experienced recruits to explore nearby areas to find new rewarding food sources after they had initially learned the exact location of the food source. Increasing the distance from the colony had no significant effect on the precision of the foraging bees. Thus, our data show that experience, but not the distance of the food source, affected the patch precision of S. mexicana foragers.