Attractiveness of single and multiple species flower patches to beneficial insects in agroecosystems

The provision of floral resources for the enhancement of beneficial insect populations has shown promise as a strategy to enhance biological control and pollination in agroecosystems. One approach involves the provision of a single flower species while a second involves the multiple flower species, but the two have never been compared experimentally. Here we examine the influence of single and multiple species flower treatments on the abundance and foraging behaviour of key beneficial insects in two agricultural agroecosystems (broccoli and lucerne crops). The five flower treatments comprised buckwheat only, phacelia only, a simple mixture of buckwheat and phacelia, a complex mixture of buckwheat, phacelia and a commercial seed blend or the existing crop as a control. The abundance of bumble‐bees (Bombus hortorum) and honey bees (Apis mellifera) was highest in the three treatments that contained phacelia, while hoverfly (Melanostoma fasciatum) numbers were high in all four flower treatments. Bumble‐bees and honey bees probed almost exclusively phacelia flowers, even when provided with a choice of other flower species in the simple and complex mixture treatments. In contrast, hoverflies probed the flowers of all plant species in single and multiple species treatments, with no apparent difference in acceptance. However, in mixture treatments, the majority of individual bumble‐bees, honey bees and hoverflies probed the flowers from only one species, despite the presence of alternative flower species. Our results illustrate how an appreciation of insect floral attractiveness can be used to customise the species composition of floral patches to potentially maximise biological control and pollination in targeted agroecosystems.     

Influence of pollinator grooming on pollen‐mediated gene dispersal in Mimulus ringens (Phrymaceae)

Pollinator foraging patterns and the dynamics of pollen transport influence the quality and diversity of flowering plant mating opportunities. For species pollinated by grooming pollinators, such as bees, the amount of pollen carried between a donor flower and potential recipient flowers depends on how grooming influences pollen transfer. To investigate the relationship between grooming and pollen‐mediated gene dispersal, we studied bumblebee (Bombus fervidus) foraging behavior and resulting gene dispersal in linear arrays of Mimulus ringens. Each of the 14 plants in an array had a unique multilocus genotype, facilitating unambiguous assignment of paternity to 1050 progeny. Each plant was trimmed to a single flower so that pollinator movements could be linked directly to resulting gene dispersal patterns. Pollen‐mediated gene dispersal was very limited. More than 95% of the seeds sired by a donor flower were distributed over the first three recipient flowers in the visitation sequence. However, seeds were occasionally sired on flowers visited later in the pollinator's floral visitation sequence. Intensive grooming immediately following pollen removal from a donor flower significantly increased the decay rate of the donor flower's gene dispersal curve. These results suggest that the frequency and relative intensity of grooming can have significant effects on patterns of pollen‐mediated gene dispersal from individual pollen donors.     

Floral display size in comfrey, Symphytum officinale L. (Boraginaceae): relationships with visitation by three bumblebee species and subsequent seed set

The fecundity of insect-pollinated plants may not be linearly related to the number of flowers produced, since floral display will influence pollinator foraging patterns. We may expect more visits to plants with more flowers, but do these large plants receive more or fewer visits per flower than small plants? Do all pollinator species respond in the same way? We would also expect foragers to move less between plants when the number of flowers per plant are large, which may reduce cross-pollination compared to plants with few flowers. We examine the relationships between numbers of inflorescence per plant, bumblebee foraging behaviour and seed set in comfrey, Symphytum officinale, a self-incompatible perennial herb. Bumblebee species differed in their response to the size of floral display. More individuals of Bombus pratorum and the nectar-robbing B.?terrestris were attracted to plants with larger floral displays, but B. pascuorum exhibited no increase in recruitment according to display size. Once attracted, all bee species visited more inflorescences per plant on plants with more inflorescences. Overall the visitation rate per inflorescence and seed set per flower was independent of the number of inflorescences per plant. Variation in seed set was not explained by the numbers of bumblebees attracted or by the number of inflorescences they visited for any bee species. However, the mean seed set per flower (1.18) was far below the maximum possible (4 per flower). We suggest that in this system seed set is not limited by pollination but by other factors, possibly nutritional resources.     

Specialist <Emphasis Type="Italic">Osmia</Emphasis> bees forage indiscriminately among hybridizing <Emphasis Type="Italic">Balsamorhiza</Emphasis> floral hosts

Pollinators, even floral generalists (=polyleges), typically specialize during individual foraging bouts, infrequently switching between floral hosts. Such transient floral constancy restricts pollen flow, and thereby gene flow, to conspecific flowers in mixed plant communities. Where incipient flowering species meet, however, weak cross-fertility and often similar floral traits can yield mixed reproductive outcomes among pollinator-dependent species. In these cases, floral constancy by polyleges sometimes serves as an ethological mating barrier. More often, their foraging infidelities instead facilitate host introgression and hybridization. Many other bee species are oligolectic (taxonomic specialists for pollen). Oligoleges could be more discriminating connoisseurs than polyleges when foraging among their limited set of related floral hosts. If true, greater foraging constancy might ensue, contributing to positive assortative mating and disruptive selection, thereby facilitating speciation among their interfertile floral hosts. To test this Connoisseur Hypothesis, nesting females of two species of oligolectic Osmia bees were presented with randomized mixed arrays of flowers of two sympatric species of their pollen host, Balsamorhiza, a genus known for hybridization. In a closely spaced grid, the females of both species preferred the larger flowered B. macrophylla, evidence for discrimination. However, both species’ females showed no floral constancy whatsoever during their individual foraging bouts, switching randomly between species proportional to their floral preference. In a wider spaced array in which the bouquets reflected natural plant spacing, foraging oligolectic bees often transferred pollen surrogates (fluorescent powders) both between conspecific flowers (geitonogamy and xenogamy) and between the two Balsamorhiza species. The Connoisseur Hypothesis was therefore rejected. Foraging infidelity by these oligolectic Osmia bees will contribute to introgression and hybridization where interfertile species of Balsamorhiza meet and flower together. A literature review reveals that other plant genera whose species hybridize also attract numerous oligolectic bees, providing independent opportunities to test the generality of this conclusion.     

Do local conspecific density and floral display size influence fruit set via pollinator visitation in Orchis militaris?

Plant density varies naturally, from isolated plants to clumped individuals, and this can influence pollinator foraging behaviour and plant reproductive success. In addition, the effect of conspecific density on reproduction may depend on the pollination system, and deceptive species differ from rewarding ones in this regard, a high density being often associated with low fruit set in deceptive plants. In our study, we aimed to determine how local conspecific density and floral display size (i.e. number of flowers per plant) affect fruit set in a deceptive orchid (Orchis militaris) through changes in pollinator visitation. We measured fruit set in a natural population and recorded pollinator abundance and foraging behaviour within plots of different O. militaris densities. Detailed data were recorded for the most abundant potential pollinators of O. militaris, i.e. solitary bees. Floral display size was negatively correlated to fruit set in medium‐density plots, but uncorrelated in low‐ and high‐density plots. Plot density had no effect on solitary bee abundance and visitation, which may be due to low pollinator abundance within the study site. The proportion of visited flowers per inflorescence was negatively influenced by floral display size, which is in line with previous studies. In addition, solitary bees spent decreasing time in successive flowers within an inflorescence, and the time spent per flower was negatively affected by ambient temperature. Our results suggest that pollinator behaviour during visitation is poorly linked to pollen deposition and reproductive success in O. militaris.     

Specialised protagonists in a plant–pollinator interaction: the pollination of Blumenbachia insignis (Loasaceae)

• Analyses of resource presentation, floral morphology and pollinator behaviour are essential for understanding specialised plant‐pollinator systems. We investigated whether foraging by individual bee pollinators fits the floral morphology and functioning of Blumenbachia insignis, whose flowers are characterised by a nectar scale‐staminode complex and pollen release by thigmonastic stamen movements.
• We described pollen and nectar presentation, analysed the breeding system and the foraging strategy of bee pollinators. We determined the nectar production pattern and documented variations in the longevity of floral phases and stigmatic pollen loads of pollinator‐visited and unvisited flowers.
• Bicolletes indigoticus (Colletidae) was the sole pollinator with females revisiting flowers in staminate and pistillate phases at short intervals, guaranteeing cross‐pollen flow. Nectar stored in the nectar scale‐staminode complex had a high sugar concentration and was produced continuously in minute amounts (~0.09 μl·h^?1). Pushing the scales outward, bees took up nectar, triggering stamen movements and accelerating pollen presentation. Experimental simulation of this nectar uptake increased the number of moved stamens per hour by a factor of four. Flowers visited by pollinators received six‐fold more pollen on the stigma than unvisited flowers, had shortened staminate and pistillate phases and increased fruit and seed set.
• Flower handling and foraging by Bicolletes indigoticus were consonant with the complex flower morphology and functioning of Blumenbachia insignis. Continuous nectar production in minute quantities but at high sugar concentration influences the pollen foraging of the bees. Partitioning of resources lead to absolute flower fidelity and stereotyped foraging behaviour by the sole effective oligolectic bee pollinator.

     

Optimal foraging: Random movement by pollen collecting bumblebees

Summary Two bumblebee species, Bombus bifarius and B. flavifrons, forage randomly with respect to direction when gathering pollen on Potentilla gracilis. Bees avoid revisiting flowers by being able to differentiate recently visited from unvisited flowers. This recognition occurs while bees are flying over open flowers and appears to be a response to the amount of available pollen within flowers. Random foraging with respect to direction is the optimal strategy when the probability of flower revisitation is low. Bumblebees appear to be moving preferentially between nearest neighbors, again as predicted by foraging theory. This behavior causes the establishment of pollen patches in the P. gracilis population. Unlike other pollinators studied in similar situations, bumblebees on P. gracilis do not forage utilizing an area-restricted searching behavior. Because floral reward quality can be assessed at low cost by bees foraging on P. gracilis, their tendency to move to nearby flowers even after encountering a poor quality blossom apparently yields a higher rate of net energy intake than does area-restricted searching. The data indicate that bumblebees exhibit great plasticity in foraging behavior and that they are able to forage efficiently under a wide range of environmental conditions.     

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.     

Determinants of foraging profitability in two nectarivorous butterflies

ABSTRACT.

• 1 I studied flower selection and foraging energetics of Agraulis vanillae L. (Nymphalidae) and Phoebis sennae (Pieridae), two butterfly species common to north central Florida. I identified the major nectar resources exploited by several populations of these butterflies and, for each plant species, measured available nectar volumes and concentrations, corolla lengths, and density. I quantified foraging behaviour of each butterfly species at each nectar source (flower visitation rate and percentage of foraging time in flight), and used these data to estimate the net rate of energy intake of each butterfly species at each nectar source.
• 2 Estimated mean energy contents of individual flowers of the eleven exploited plant species spanned three orders of magnitude, ranging between 0.015 and 9.27 joules. Mean energy content of individual flowers was strongly correlated with mean foraging profit of both butterfly species.
• 3 Mean nectar volume strongly influenced energy content and varied widely within and among species, ranging from 0.0076 to 1.853 μ1. Nectar concentration varied between 17.1% and 40.4% sucrose-equivalents. Nectar volume was the best single predictor of foraging profitability (correlation coefficients of 0.994 and 0.984 for Phoebis and Agraulis respectively). Corolla length also strongly affected foraging profitability for both butterfly species; flower species with longer corollas were generally more profitable.
• 4 Flower density and nectar concentration showed weak or nonsignificant associations with foraging profitability.
• 5 The usefulness and limitations of these floral characteristics as bases for foraging selectivity, and the selective pressures foraging butterflies might place on the visited plants are discussed.

     

Solitary and social bees as pollinators of Wahlenbergia (Campanulaceae): single-visit effectiveness, overnight sheltering and responses to flower colour

Solitary bees often form specialised mutualisms with particular plant species, while honeybees are considered to be relatively opportunistic foragers. Thus, it may be expected that solitary bees are more effective pollinators than honeybees when foraging on the same floral resource. To test this, we studied two Wahlenbergia species (Campanulaceae) in South Africa that are visited by both social honeybees and solitary bees, and which are shown here to be genetically self-incompatible and thus reliant on pollinator visits for seed production. Contrary to expectation, the solitary bee Lipotriches sp. (Halictidae) and social bee Apis mellifera (Apidae), which were the two most frequent visitors to flowers of the study species, were equally effective pollinators in terms of the consequences of single visits for fruit and seed set. Both bee species preferentially visited female phase flowers, which contain more nectar than male phase flowers. Male solitary bees of several genera frequently shelter overnight in flowers of both Wahlenbergia species, but temporal exclusion experiments showed that this behaviour makes little contribution to either seed production or pollen dispersal (estimated using a dye particle analogue). Manipulation of flower colour using a sunscreen that removed UV reflectance strongly reduced visits by both bee groups, while neither group responded to Wahlenbergia floral odour cues in choice tests. This study indicates that while flowers of Wahlenbergia cuspidata and W. krebsii are pollinated exclusively by bees, they are not under strong selection to specialise for pollination by any particular group of bees.     

Buzz pollination in eight bumblebee-pollinated Pedicularis species: does it involve vibration-induced triboelectric charging of pollen grains?

MethodsEight sympatric buzz-pollinated species of Pedicularis that share bumblebee pollinator species were studied, giving a rare opportunity to compare sonication behaviour of a shared pollinator on different plant species.ConclusionsSonication behaviour of B. friseanus differs among Pedicularis species, not only because worker bees assort themselves among plant species by body size, but also because bees of a given size adjust the buzz frequency to achieve a vibration velocity corresponding to the floral traits of each plant species. These findings, and the floral traits that characterize these and other buzz-pollinated species, are compatible with the hypothesis of vibration-induced triboelectric charging of pollen grains.     

The movement patterns of carpenter beesXylocopa micans and bumblebeesBombus pennsylvanicus onPontederia cordata inflorescences

The movement patterns of carpenter bees (Xylocopa micans) and bumblebees (Bombus pennsylvanicus) foraging for nectar on vertical inflorescences ofPontederia cordata were studied near Miami, Florida. The floral biology ofP. cordata is unique in several ways: (a) many short-lived flowers per inflorescence, (b) constant nectar production throughout the life span of each flower, and (c) abscence of vertical patterning of nectar and age of flowers. Inflorescences ranged between 3.5 and 15.8 cm long and had between 9 and 55 open flowers. Both carpenter bees and bumblebees arrived mostly on the bottom third of the inflorescence and left after visiting flowers on the top third of the inflorescence. The departure position from the inflorescence was higher up than observed in studies of other insect pollinators foraging on other speces of plants. This pattern of departure probably occurs in the absence of a vertical gradient of nectar or floral morphology.     

Floral Sonication is an Innate Behaviour in Bumblebees that can be Fine-Tuned with Experience in Manipulating Flowers

Bumblebees demonstrate an extensive capacity for learning complex motor skills to maximise exploitation of floral rewards. This ability is well studied in nectar collection but its role in pollen foraging is less well understood. Floral sonication is used by bees to extract pollen from some plant species with anthers which must be vibrated (buzzed) to release pollen. Pollen removal is determined by sonication characteristics including frequency and amplitude, and thus the ability to optimise sonication should allow bees to maximise the pollen collection. We investigated the ability of the buff-tailed bumblebee (Bombus terrestris) to modify the frequency and amplitude of their buzzes with increasing experience manipulating flowers of the buzz-pollinated plant Solanum rostratum. We analysed flight and feeding vibrations generated by naïve workers across feeding bouts. Feeding buzzes were of a higher frequency and a lower amplitude than flight buzzes. Both flight and feeding buzzes had reduced amplitudes with increasing number of foraging trips. However, the frequency of their feeding buzzes was reduced significantly more than their flight buzzes as bumblebee workers gained experience manipulating flowers. These results suggest that bumblebees are able to modify the characteristics of their buzzes with experience manipulating buzz-pollinated flowers. We discuss our findings in the context of bumblebee learning, and the current understanding of the optimal sonication characteristics for releasing pollen in buzz-pollinated species. Our results present a tantalising insight into the potential role of learning in floral sonication, paving the way for future research in this area.     

Intra‐floral resource partitioning between endemic and invasive flower visitors: consequences for pollinator effectiveness

1. Sympatric flower visitor species often partition nectar and pollen and thus affect each other's foraging pattern. Consequently, their pollination service may also be influenced by the presence of other flower visiting species. Ants are solely interested in nectar and frequent flower visitors of some plant species but usually provide no pollination service. Obligate flower visitors such as bees depend on both nectar and pollen and are often more effective pollinators. 2. In Hawaii, we studied the complex interactions between flowers of the endemic tree Metrosideros polymorpha (Myrtaceae) and both, endemic and introduced flower‐visiting insects. The former main‐pollinators of M. polymorpha were birds, which, however, became rare. We evaluated the pollinator effectiveness of endemic and invasive bees and whether it is affected by the type of resource collected and the presence of ants on flowers. 3. Ants were dominant nectar‐consumers that mostly depleted the nectar of visited inflorescences. Accordingly, the visitation frequency, duration, and consequently the pollinator effectiveness of nectar‐foraging honeybees (Apis mellifera) strongly decreased on ant‐visited flowers, whereas pollen‐collecting bees remained largely unaffected by ants. Overall, endemic bees (Hylaeus spp.) were ineffective pollinators. 4. The average net effect of ants on pollination of M. polymorpha was neutral, corresponding to a similar fruit set of ant‐visited and ant‐free inflorescences. 5. Our results suggest that invasive social hymenopterans that often have negative impacts on the Hawaiian flora and fauna may occasionally provide neutral (ants) or even beneficial net effects (honeybees), especially in the absence of native birds.     

Inflorescence Height Affects Visitation Behavior of Bees–A Case Study of an Aquatic Plant Community in Bolivia1

We studied the bee fauna visiting a plant community of 10 species of flowering aquatic plants in an inundated savanna region in Bolivia. In total we observed 36 bee species in 17 genera at the flowers. Cluster analysis of the similarities among the plant species in terms of their visitor spectra showed a division into two groups: plants with inflorescence heights shorter than the grass height and plants with inflorescences projecting out of the surrounding vegetation. Larger bees of the genera Apis, Melipona, Bombus, and Xylocopa were observed only at flowers above the surrounding vegetation. Smaller, mainly solitary bees (e.g., Augochlorella, Ancyloscelis) visited flowers in the dense vegetation near the water surface. Analyses of the pollen loads revealed that most individuals were highly flower constant. When bees carried different pollen types, it was generally pollen from flowers within a single stratum. We discuss specialization, flower constancy, competition, and different foraging strategies as possible reasons for stratum fidelity.     

Caste-specific patterns of flower visitation in bumble bees (Bombus kirbyellus) collecting nectar from Polemonium viscosum

ABSTRACT.

• 1 Foraging routes of worker and queen bumble bees (Bombus kirbyellus Curtis) collecting nectar from flowers of the alpine sky pilot, Polemonium viscosum Nutt., were followed and the corolla tube length, corolla diameter, floral scent, and number of flowers on plants visited or bypassed by bees were monitored. Additionally, the number and proportion of flowers visited per inflorescence and distance flown from each to the next were recorded. Queens and workers differed significantly in choice of flowers. However, intra-inflorescence visitation rates and departure distances were similar between castes. Castes differed in the extent to which visitation reflected patch quality versus individual floral traits.
• 2 Both queens and workers failed to visit skunky-flowered plants more often than they failed to visit sweet-flowered ones, and preferred large over small inflorescences. However, queens visited large-flowered plants more often than small-flowered ones, while workers preferred flowers with shorter corolla tubes, regardless of their diameter. Although a number of studies have documented caste specialization on alternate species of host plants, ours is one of the first to show that morphological preferences promote comparable foraging differences between castes on monospecific plant resources.
• 3 Queens, once on a plant, responded to floral traits by probing more flowers on large inflorescences, as well as on those with broader floral form. Workers did not alter intra-inflorescence visitation rate in response to floral traits.
• 4 For workers, no significant relationship was demonstrated between the likelihood of passing by a plant and the number of flowers probed on the previous inflorescence visited. Thus, workers appeared to accept or reject each plant of P. viscosum independently. However, queens passed by fewer plants when leaving rich inflorescences than poor ones. These results suggest that workers use only individual plant acceptability in choosing which plants to visit, whereas queens base plant choice on patch and individual attributes. Such differences between castes in foraging rules when exploiting the same floral resource have received little attention, and provide insights into the heterogeneity of harvestable reward distributions from the perspective of the forager population.

     

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.     

Pollination biology in Roepera (Zygophyllaceae): How flower structure and shape influence foraging activity

The foraging behavior of bees is a complex phenomenon that depends on numerous physical features of flowers. Of particular importance are accessibility of floral rewards, floral proportions, symmetry and orientation. The flowers of Roepera are characterized by the presence of staminal scales (SS), which play an important role in nectar protection. We studied two species of Roepera with different symmetry and flower orientation, which are mainly visited by honeybees (Apis mellifera). We aimed to show how the foraging behavior of honey bees is affected by the function of SS, floral symmetry and orientation. The foraging behavior was documented by video photography. Handling time, access to nectar, percentage of pollen/nectar foraging, percentage of pollen contact and pollen deposition site on the honey bee's body were assessed. The morphometric features of the honey bees and flowers were analyzed. We found that the SS restricted pollinator access to nectar. Our results indicated consistency of visitation patterns in zygomorphic, laterally oriented flowers of R. fuscata versus random patterns in actinomorphic, diversely oriented flowers of R. leptopetala. The relative proportions of SS and proboscis length appear to be crucial for the success of pollinators. The directionality of the honey bees' movement, together with the different positioning of reproductive organs, plays an important role in the accuracy of pollen transfer and pollination efficiency.     

Floral visitors and ant scent marks: noticed but not used?

1. Bee behaviour when visiting flowers is mediated by diverse chemical cues and signals, from the flower itself and from previous visitors to the flower. Flowers recently visited by bees and hoverflies may be rejected for a period of time by subsequent bee visitors. 2. Nectar‐thieving ants also commonly visit flowers and could potentially influence the foraging decisions of bees, through the detection of ant trail pheromones or footprint hydrocarbons. 3. Here we demonstrate that, while naÏve bumblebees in laboratory trials are not inherently repelled by ant scent marks, they can learn to use them as informative signals while foraging on artificial flowers. 4. To test for similar activity in the wild, visitor behaviours at the flowers of Digitalis purpurea Linnaeus, Bupleurum fruticosum Linnaeus, and Brassica juncea (Linnaeus) Czernajew were compared between flowers that had been in contact with ants and those that had not. No differences were found between the two treatments. 5. The use of chemical foraging cues by bees would appear to be strongly dependent on previous experience and in the context of these plant species bees did not associate ant scent mark cues with foraging costs.     

Interaction between oil-collecting bees and seven species of Plantaginaceae

Oil-bee/oil-flower mutualism evolved through multiple gains and losses of the ability to produce floral oil in plants and to collect it in bees. Around 2000 plant species are known to produce floral oils that are collected by roughly 450 bee species, which use them for the construction of nests and for the larval food. The Plantaginaceae contain several Neotropical species that produce floral oils, the main reward offered by these plants. In the genera Angelonia, Basistemon, Monopera and Monttea, mainly associated with Centris bees, the floral oil is produced in trichomes that are located in the inner corolla. The pollinators of a few species in this neotropical clade of Plantaginaceae are known, and the role of flower morphology as well as the requirements from pollinators and the role of other groups of bees in the pollination of these flowers remains unclear. In this paper we provide a list of the flower visitors of seven Plantaginaceae species (six Angelonia species and Basistemon silvaticus) analyzing their behavior to highlight the legitimate pollinators and illustrating little known aspects of flower morphology and oil-collecting apparatuses of the bees. Two general morphological patterns were observed in the Angelonia flowers: deep corolla tube with short lobes, and short corolla tube with long lobes. Corolla tubes of different length result in pollen adherence to different parts of the insect body. The six Angelonia species and B. silvaticus flowers were visited by 25 oil-collecting bee species (10 Centris, 11 Tapinotaspidini and 4 Tetrapedia species), the majority acting as legitimate visitors. The flowers were also visited by illegitimate bee pollinators, which collected pollen but do not transfer it to the female organ. Specialized collectors of Plantaginaceae floral oils present modifications on the first pair of legs, mainly in the basitarsi but also extended to the tarsomeres. The new records of Tapinotaspidini and Centridini species acting as specialized pollinators of Plantaginaceae suggest that there is a geographic variation in the pollinators of the same plant species, and that the evolutionary scenario of the historical relationships between oil-collecting bees and floral oil producing plants is more complex than previously considered.