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.     

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.     

Why do honeybees reject certain flowers?

Summary Honeybees often approach flowers of Lotus corniculatus and then fly away without attempting to extract nectar. These rejected flowers contained 41% less nectar than my random sample. The accepted flowers contained 24% more nectar than my random sample. The differences among these three flower-groups were due to differences in the percent of empty flowers in each group rather than the differences in the absolute amount of nectar. Honeybees increased their foraging efficiency by accepting less empty flowers and rejecting more empty flowers than would be expected if they foraged randomly. There are two possible mechanisms for this discrimination-behavior: either the bees are smelling nectar odor or they are smelling bee scent left by previous visitors to the flower. My results are inconsistent with the hypothesis that bees are basing their decision on nectar smell and suggest that they are using bee scent as a means of identifying empty flowers.     

The repellent scent-mark of the honeybeeApis mellifera tigustica and its role as communication cue during foraging

Summary Experimental evidence for flower-marking in honeybees (Apis mellifera ligustica), using pairs of workers from the same colony foraging on an artificial patch of flowers, is reported. Workers marked artificial flowers with scent and strongly rejected all flowers they had recently visited. The same rejection behavior, in a lower although significant proportion, was observed when bees visited flowers just abandoned by the other individual of the pair. The repellent nature of this scent-mark was demonstrated with the use of an air extractor connected to the patch of artificial flowers. When the apparatus was turned on, the rejection behavior disappeared and bees accepted both flowers just abandoned by themselves and flowers just abandoned by the other bee. Differences in the response level of bees to their own marks or to the partner's marks suggest that the repellent scent-mark applied by a bee during foraging would basically be a self-use signal, although it certainly has value in communicating with other workers.     

Are pollination syndromes useful predictors of floral visitors in Tasmania?

Abstract Diurnal visitors to the flowers of many native plant species were identified in a wide range of Tasmanian sclerophyllous vegetation between September 1996 and April 1997. These foraging profiles were analysed to determine whether they were characteristic of various floral morphologies in predictable ways. It was found that although visitor profiles were sometimes consistent with classic pollination syndromes, these syndromes were unreliable predictors of floral visitors. Very few flowers were exclusively bird‐pollinated, and none were strictly fly‐, beetle‐, wasp‐, or butterfly‐pollinated. The majority of flowering plants were unspecialized in their morphology, and consequently hosted a diverse array of visitors. In addition, visitor profiles to congeners with similar floral morphologies, and even to conspecifics, differed between habitats. Altitude was a major factor in determining visitors, with flies being the most abundant visitors above 700 m. However, congeners in several genera of Epacridaceae, as well as the genus Correa, which differed in floral morphology also differed in visitor profiles. Tubular flowers were associated with birds, while flowers with more accessible nectar were visited by insects. The only taxa exhibiting a bee‐pollination syndrome that were largely visited by bees were the Fabaceae and Goodenia ovata Sm. Several species with purple or pink flowers were also predominantly visited by bees, but did not strictly conform to the melittophilous syndrome. In contrast, other flowers exhibiting an ostensibly mellitophilous syndrome hosted very few bees. Of these, species that occurred at high altitude were mainly visited by flies, while others received very few potential pollen vectors.     

Pollination of Campomanesia phaea (Myrtaceae) by night‐active bees: a new nocturnal pollination system mediated by floral scent

• Bees are the most important diurnal pollinators of angiosperms. In several groups of bees a nocturnal/crepuscular habit developed, yet little is known about their role in pollination and whether some plants are adapted specifically to these bees. We used a multidisciplinary approach to investigate the reproductive biology and to understand the role of nocturnal/crepuscular bees in pollination of Campomanesia phaea (Myrtaceae), popularly named cambuci.
• We studied the floral biology and breeding system of C. phaea. We collected the floral visitors and tested the pollinators' effectiveness. We also determined the floral scents released at night and during daytime, and studied behavioural responses of crepuscular/nocturnal bees towards these scents.
• The flowers of cambuci were self‐incompatible and had pollen as the only resource for flower visitors. Anthesis lasted around 14 h, beginning at 04:30 h at night. The flowers released 14 volatile compounds, mainly aliphatic and aromatic compounds. We collected 52 species of floral visitors, mainly bees. Nocturnal and crepuscular bees (four species) were among the most frequent species and the only effective pollinators. In field bioassays performed at night, nocturnal/crepuscular bees were attracted by a synthetic scent blend consisting of the six most abundant compounds.
• This study describes the first scent‐mediated pollination system between a plant and its nocturnal bee pollinators. Further, C. phaea has several floral traits that do not allow classification into other nocturnal pollination syndromes (e.g. pollinator attraction already before sunrise, with pollen as the only reward), instead it is a plant specifically adapted to nocturnal bees.

     

Visual and Olfactory Floral Cues of Campanula (Campanulaceae) and Their Significance for Host Recognition by an Oligolectic Bee Pollinator

Oligolectic bees collect pollen from a few plants within a genus or family to rear their offspring, and are known to rely on visual and olfactory floral cues to recognize host plants. However, studies investigating whether oligolectic bees recognize distinct host plants by using shared floral cues are scarce. In the present study, we investigated in a comparative approach the visual and olfactory floral cues of six Campanula species, of which only Campanula lactiflora has never been reported as a pollen source of the oligolectic bee Ch. rapunculi. We hypothesized that the flowers of Campanula species visited by Ch. rapunculi share visual (i.e. color) and/or olfactory cues (scents) that give them a host-specific signature. To test this hypothesis, floral color and scent were studied by spectrophotometric and chemical analyses, respectively. Additionally, we performed bioassays within a flight cage to test the innate color preference of Ch. rapunculi. Our results show that Campanula flowers reflect the light predominantly in the UV-blue/blue bee-color space and that Ch. rapunculi displays a strong innate preference for these two colors. Furthermore, we recorded spiroacetals in the floral scent of all Campanula species, but Ca. lactiflora. Spiroacetals, rarely found as floral scent constituents but quite common among Campanula species, were recently shown to play a key function for host-flower recognition by Ch. rapunculi. We conclude that Campanula species share some visual and olfactory floral cues, and that neurological adaptations (i.e. vision and olfaction) of Ch. rapunculi innately drive their foraging flights toward host flowers. The significance of our findings for the evolution of pollen diet breadth in bees is discussed.     

Intrafloral patterns of color and scent in Capparis spinosa L. and the ghosts of its selection past

Premise

Capparis spinosa is a widespread charismatic plant, in which the nocturnal floral habit contrasts with the high visitation by diurnal bees and the pronounced scarcity of hawkmoths. To resolve this discrepancy and elucidate floral evolution of C. spinosa, we analyzed the intrafloral patterns of visual and olfactory cues in relation to the known sensory biases of the different visitor guilds (bees, butterflies, and hawkmoths).

Methods

We measured the intrafloral variation of scent, reflectance spectra, and colorimetric properties according to three guilds of known visitors of C. spinosa. Additionally, we sampled visitation rates using a motion-activated camera.

Results

Carpenter bees visited the flowers eight times more frequently than nocturnal hawkmoths, at dusk and in the following morning. Yet, the floral headspace of C. spinosa contained a typical sphingophilous scent with high emission rates of certain monoterpenes and amino-acid derived compounds. Visual cues included a special case of multisensory nectar guide and color patterns conspicuous to the visual systems of both hawkmoths and bees.

Conclusions

The intrafloral patterns of sensory stimuli suggest that hawkmoths have exerted strong historical selection on C. spinosa. Our study revealed two interesting paradoxes: (a) the flowers phenotypically biased towards the more inconsistent pollinator; and (b) floral display demands an abundance of resources that seems maladaptive in the habitats of C. spinosa. The transition to a binary pollination system accommodating large bees has not required phenotypic changes, owing to specific eco-physiological adaptations, unrelated to pollination, which make this plant an unusual case in pollination ecology.     

Pollination in Turnera subulata (Turneraceae): Unilateral reproductive dependence of the narrowly oligolectic bee Protomeliturga turnerae (Hymenoptera, Andrenidae)

Turnera subulata Smith (Turneraceae) is a subshrub with distylic flowers, common as a ruderal plant in NE-Brazil. We studied the pollination biology of a population in João Pessoa, Paraíba, paying attention to effective pollinators and characteristics of short- and long-style morphs. The flowers attracted insects of 28 species, predominantely bees. Several bee species were observed to be effective pollinators, including highly eusocial species, polylectic solitary species (Centris and Xylocopa) and 1 oligolectic species, Protomeliturga turnerae (Andrenidae, Panurginae). The latter species shows reproductive dependency on T. subulata. The plant species, on the other hand, does not depend on this specialized bee, as reproductive success was also guaranteed by the other polylectic flower visitors. Floral characteristics of both floral morphs are discussed with respect to pollination biology.     

Faunal makeup of wild bees and their flower utilization in a semi-urbanized area in central Japan

The species composition of wild bees and their flower utilization patterns were surveyed from April to November in 1996 in a semi‐urbanized area adjacent to Sugao Marsh, Ibaraki, central Japan. A total of 750 individuals belonging to 43 species in six families were collected. The most dominant family was Halictidae, for which 13 species and 251 individuals were collected. The most dominant species was Colletes patellatus (120 individuals) of the Colletidae. The results at Sugao were compared with those obtained from three other areas of Ibaraki Prefecture, which have similar climatic conditions, yet have different environmental characteristics in terms of human impact. The four sites in Ibaraki can be classified into two groups: the first comprising Sugao and Mito in cultivated and/or human‐dwelling areas, and the second comprising Yamizo and Gozen’yama, in forest areas with more natural elements. The number of species at Sugao was the smallest among the four study sites. On the other hand, the values for species evenness at Sugao were the second‐highest of the four study sites. These findings show that the different characteristics of different bee communities reflect their local environmental conditions, including their floral compositions. The bees visited 36 flower species in 20 families, and 70.7% of all individuals studied visited Compositae flowers. The heavy utilization of composite flowers is possibly because of the existence of a simplified flora consisting of a few dominant composite plant species. Among these plants, Solidago altissima and Lactuca indica made large contributions to supporting autumn bees, especially Colletes patellatus and Colletes perforator, which are solitary and oligolectic on Compositae.     

Bees visiting flowers of Thymus longicaulis (Lamiaceae)

The aim of this study was to investigate the bee fauna foraging on Thymus longicaulis flowers. Samplings were conducted walking along a transect during the T. longicaulis blooming period (April–June). A total of 547 bee specimens, belonging to 40 different species, were recorded during the survey. Apis mellifera and Bombus terrestris were the most abundant visitors that foraged on thyme. Pollen grains collected on the bodies of the bees suggest that these pollinators may play an important role in the pollination of this plant.     

Discrimination of Unrewarding Flowers by Bees; Direct Detection of Rewards and Use of Repellent Scent Marks

Bumblebees and honeybees deposit short-lived scent marks on flowers that they visit when foraging. Conspecifics use these marks to distinguish those flowers that have recently been emptied and, so, avoid them. The aim of this study was to assess how widespread this behavior is. Evidence for direct detection of reward levels was found in two bee species: Agapostemon nasutus was able to detect directly pollen availability in flowers with exposed anthers, while Apis mellifera appeared to be able to detect nectar levels of tubular flowers. A third species, Trigona fulviventris, avoided flowers that had recently been visited by conspecifies, regardless of reward levels, probably by using scent marks. Three further bee/flower systems were examined in which there was no detectable discrimination among flowers. We argue that bees probably rely on direct detection of rewards where this is allowed by the structure of the flower and on scent marks when feeding on flowers where the rewards are hidden. However, discrimination does not always occur. We suggest that discrimination may not always make economic sense; when visiting flowers with a low handling time, or flowers that are scarce, it may be more efficient to visit every flower that is encountered.     

Anthecology of Orchis mascula (Orchidaceae)

Interactions between Orchis mascula L. ssp. mascula and anthophilous insects were studied mainly on the island of Öland, Sweden. The species is nectarless and acts by deceiving various bees (Hymenoptera, Apoidea). Temporary seeking/exploratory drives of bees for food–sources were exploited by means of superiority in floral display. A floral reflectance maximum at 440 nm (blue) largely determines the colour in the visual spectrum of bees. The floral scent is composed to about 90% of mono–terpenes. Nothing suggested mimesis of concurrent food–flowers either in colour or in scent. Anthesis covered a time period in late spring when (a) concurrent food–flowers for bees were rather few, (b) many bumble–bee queens (Bombus Latr. spp.) were inexperienced as regards food–flowers and had no foraging routines, (c) cuckoo bumble–bee females (Psithyrus Lep. spp.) recovery–fed on flowers after hibernation, (d) males of Eucera longicornis (L.) (Anthophoridae) patrolled far out from their nest–area, and when (e) many solitary bee species flew about. The pollinator fauna differed between sites, viz. either Bombus queens, Psithyrus females or E. longicornis males transported the majority of the pollinaria. The pollination system does not seem to be stabilised in the study areas. Floral morphology indicates that the plant's anthecological specialisation to bees as a group implies a graded unspecialisation to each species of bee in the legitimate pollinator group.     

Pollination ofEchinocereus fasciculatus andFerocactus wislizenii

One of the most common types of cactus flower in the southwestern United States is the large, colorful, cup-shaped flower.Echinocereus fasciculatus var.boyce-thompsonii in Arizona is a representative of this class of flowers. Its flowers are visited by three common types of insect visitors: medium-sized bees, small solitary bees, and beetles. All three types of visitors come into contact with the pollen, but only the mediumsized bees regularly touch the stigma in their visitations. The main effective pollinators are therefore the medium-sized bees (Megachile, etc.).Ferocactus wislizenii has a similar floral mechanism and is likewise pollinated mainly by medium-sized bees (Megachile, Lithurge, Diadasia, etc.).Pollination of North American Cacti, 1.     

Bees use honest floral signals as indicators of reward when visiting flowers

Pollinators visit flowers for rewards and should therefore have a preference for floral signals that indicate reward status, so called ‘honest signals’. We investigated honest signalling in Brassica rapa L. and its relevance for the attraction of a generalised pollinator, the bumble bee Bombus terrestris (L.). We found a positive association between reward amount (nectar sugar and pollen) and the floral scent compound phenylacetaldehyde. Bumble bees developed a preference for phenylacetaldehyde over other scent compounds after foraging on B. rapa. When foraging on artificial flowers scented with synthetic volatiles, bumble bees developed a preference for those specific compounds that honestly indicated reward status. These results show that the honesty of floral signals can play a key role in their attractiveness to pollinators. In plants, a genetic constraint, resource limitation in reward and signal production, and sanctions against cheaters may contribute to the evolution and maintenance of honest signalling.     

Echium and Pontechium specific floral cues for host–plant recognition by the oligolectic bee Hoplitis adunca

Flowering plants often have specific floral cues, which allow bees and other pollinators to differentiate between them. Many bee species exhibit specialised associations with flowers (oligolecty) and it is important for them to find and recognise their specific host plants. In this study we compared the visual and olfactory floral cues of different Echium and Pontechium (Boraginaceae) species with the closely related Anchusa officinalis (Boraginaceae). We tested whether plant-specific cues occur in Echium and Pontechium which may allow oligolectic Hoplitis adunca (Megachilidae) to recognise its host plants and to distinguish them from Anchusa non-hosts. Our investigations showed that Echium/Pontechium provides a specific scent bouquet. Furthermore, we identified compounds which were not described as floral scent before ((Z)-3-nonenal and 1,4-benzoquinone). These unique volatiles and the specific bouquet could act as a recognition cue for H. adunca. The corolla colours differed between all species, but were grouped together in the bee colour categories blue and UV-blue and can indicate potential host flowers for H. adunca.     

Individually recognizable scent marks on flowers made by a solitary bee

The marking of flowers with ephemeral scent is an underappreciated but vital element in the foraging behaviour of social bees. Using observational and experimental data, we tested whether a solitary bee (female Anthophora plumipes) uses scent marking while foraging on flowers of Cerinthe major in Portugal. Females used scent marks with at least two components that differed in their volatility and, furthermore, recognized the marks of different individuals. A very short-term component (<3 min) was attractive, resulting in the observed high level of immediate revisits: this component appeared to be adjusted according to the foraging needs of the moment. A longer-term component (<30 min) was initially repellent and matched the rate of nectar renewal; it, or the response to it, also appeared to be adjusted to the perceived level of nectar reward. There may be even longer-term effects associated with the specific foraging areas of individual bees. Observed differences in the way in which individuals responded to scent marks indicate that they may play a role as part of a dominance or exclusion mechanism among females. Copyright 2001 The Association for the Study of Animal Behaviour.     

Morning floral heat as a reward to the pollinators of the Oncocyclus irises

Relationships between flowering plants and their pollinators are usually affected by the amount of reward, mainly pollen or nectar, offered to pollinators by flowers, with these amounts usually positively correlated with floral display. The large Oncocyclus iris flowers, despite being the largest flowers in the East Mediterranean flora, are nectarless and have hidden pollen. No pollinators visit the flowers during daytime, and these flowers are pollinated only by night-sheltering solitary male bees. These iris flowers are partially or fully dark-colored, suggesting that they gather heat by absorbing solar radiation. Here we test the hypothesis that the dark-colored flowers of the Oncocyclus irises offer heat reward to their male solitary bee pollinators. Floral temperature was higher by 2.5°C than ambient air after sunrise. Solitary male bees emerged earlier after sheltering in Oncocyclus flowers than from other experimental shelter types. Pollination tunnels facing east towards the rising sun hosted more male bees than other aspects. We suggest that floral heat reward can explain the evolution of dark floral colors in Oncocyclus irises, mediated by the pollinators’ behavior.     

Species and subspecies specificity in urine and scent marks of saddle-back tamarins (Saguinus fuscicollis)

Saguinus fuscicollisproduces scent marks which consist mainly of a mixture of urine and the secretions of circumgenital scent glands. The present study investigates the ability of saddle-back tamarins to discriminate between scent material from conspecifics and corresponding material from other species and to differentiate material from two subspecies of Saguinus fuscicollis.When choices between urine samples from conspecifics and from guinea pigs and choices between urine samples from conspecifics and from common marmosets were offered, the tamarins investigated samples from conspecifics more frequently. Similar responses were obtained when choices between scent marks from saddle-back tamarins and from common marmosets and between scent marks from saddle-back and red-chested moustached tamarins were offered. The tamarins also discriminated between scent marks and between extracts of scent marks from Saguinus f. fuscicollisand Saguinus f. illigeri.In these choice tests, subjects of both subspecies tended preferentially to investigate material from Saguinus f. fuscicollis.The results of these studies show that urine and scent marks contain chemical cues on which recognition of conspecifics can be based. Moreover, the scent marks of closely related subspecies also offer cues which could enable the tamarins to discriminate between them.     

Predation Cues in Solitary bee Nests

Predation at the nesting site can significantly affect solitary bees’ reproductive success. We tested female red mason bees’ (Osmia bicornis L.) acceptance of potential nesting sites, some of which were marked with cues coming from predated conspecifics (crushed bees) or from a predator itself (rodent excreta). In our experiment, females did not avoid nests marked with either of the two predator cues. We suggest that bee females do not recognize these two cues as risky. Alternatively, costs of abandoning natal aggregation might be too high compared with any perceived predation risk of staying. Moreover, the presence of crushed bees can provide positive information about the presence of conspecifics and, possibly, information about a nesting aggregation that may be preferred by bees when choosing a nesting site.