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.     

Pollination of four sympatric species ofAngelonia (Scrophulariaceae) by oil-collecting bees in NE. Brazil

The manner whereby the oil-producing bisaccate flowers ofAngelonia (Scrophulariaceae) are pollinated by female oil-collecting bees is reported for the first time. Observations were made in the Caatinga formation of Pernambuco, NE. Brazil, on four synchronopatric species. These differ in sizes and structural details of the corolla, level of flower exposition, and habitat preferences. All legitimate visitors wereCentris spp. (Anthophoridae):Angelonia hirta was mainly pollinated byC. fuscata andA. pubescens byC. hyptidis; A. bisaccata andA. hookeriana shared an unidentified species. Several exomalopsine, tetrapediine and meliponid bees exploit the flowers less descriminately for oil or pollen, respectively, without regularly contacting anthers and stigma. The flowers are protandrous, and are self-incompatible except those of the annualA. pubescens. After alighting, theCentris bees introduce their front legs simultaneously into each of the pouches and start alternate collecting movements to gather the oil from the trichome elaiophores. While doing so, they are forced by projections of the corolla floor to press their head under the anthers and stigma, whereby pollen is transferred with their frons or clypeus. On account of their collector type and behaviour,C. fuscata andC. spec. are not specialized toAngelonia but may equally exploit other nonrelated taxa for oil, whereasC. hyptidis exhibits oligolecty onA. pubescens. It possesses relatively elongate forelegs with padlike collectors suitable for sweeping the lipids from the scattered glandular hairs inside the divergent spurs of its host. It is the only species that also collects pollen (by buzzing) from the oil host.A. hirta and relatives, provided with dense elaiophore carpets, are, for their part, adapted to scrapingCentris species with typical oil collectors. Flower and bee phenologies, although largely dependent on the irregular rainfalls, are not always coincident.     

HasIxianthes (Scrophulariaceae) lost its special bee?

Ixianthes retzioides is a rare, moderately sized, shrub with large yellow flowers that are lined with glandular trichomes. Preliminary analysis indicates that the trichomes secrete a complex mixture of lipids. Floral morphology suggests thatIxianthes should be pollinated by a large oil-collecting bee, yet only one possible candidate,Rediviva gig, is known and it occurs outside of the distributional range ofIxianthes. Despite observations ofIxianthes at different sites in different years, no oil-collecting bee has been observed visiting the flowers. This together with low fruit and seed set at the main study site suggests thatIxianthes has lost, at least locally, its specialized pollinator. Plants are self-compatible and set a limited amount of seed as a result of visits by pollen-collecting bees.     

The consequences of specialization for pollination in a rare South African shrub,Ixianthes retzioides (Scrophulariaceae)

Ixianthes retzioides is a rare South African shrub with large yellow oil-secreting flowers. Populations studied previously revealed low levels of reproductive success and the absence of a specialized oil-collecting pollinator. We report the discovery of a population in which the predicted specialist pollinator,Rediviva gigas, is present. The presence of this oil-collecting bee resulted in a mean fruit set per plant of 97.2 ± 8.3% (N = 9) and a mean seed set of 331.6 ± 162.6 (N = 52). This represents a 7.4-fold increase in fruit set and a 7.8-fold increase in seed set over a previously studied population lacking the specialist pollinator. The contrast between populations with and without the specialist pollinator dramatically illustrates the potential benefits and costs of specialization for pollination, respectively.     

Pterandra pyroidea: a case of pollination shift within neotropical Malpighiaceae

Background and Aims

Most Neotropical species of Malpighiaceae produce floral fatty oils in calyx glands to attract pollinating oil-collecting bees, which depend on this resource for reproduction. This specialized type of pollination system tends to be lost in members of the family that occur outside the geographic distribution (e.g. Africa) of Neotropical oil-collecting bees. This study focused on the pollination ecology, chemical ecology and reproductive biology of an oil flower species, Pterandra pyroidea (Malpighiaceae) from the Brazilian Cerrado. Populations of this species consist of plants with oil-secreting (glandular) flowers, plants with non-oil-secreting flowers (eglandular) or a mix of both plant types. This study specifically aims to clarify the role of eglandular morphs in this species.

Methods

Data on pollinators were recorded by in situ observations. Breeding system experiments were conducted by isolating inflorescences and by enzymatic reactions. Floral resources, pollen and floral oils offered by this species were analysed by staining and a combination of various spectroscopic methods.

Key Results

Eglandular flowers of P. pyroidea do not act as mimics of their oil-producing conspecifics to attract pollinators. Instead, both oil-producing and oil-free flowers depend on pollen-collecting bees for reproduction, and their main pollinators are bumble-bees. Floral oils produced by glandular flowers are less complex than those described in closely related genera.

Conclusions

Eglandular flowers represent a shift in the pollination system in which oil is being lost and pollen is becoming the main reward of P. pyroidea flowers. Pollination shifts of this kind have hitherto not been demonstrated empirically within Neotropical Malpighiaceae and this species exhibits an unusual transition from a specialized towards a generalized pollination system in an area considered the hotspot of oil-collecting bee diversity in the Neotropics. Transitions of this type provide an opportunity to study ongoing evolutionary mechanisms that promote the persistence of species previously involved in specialized mutualistic relationships.     

Foraging behavior of three bee species in a natural mimicry system: female flowers which mimic male flowers in Ecballium elaterium (Cucurbitaceae)

Summary The behavior of Apis mellifera and two species of solitary bees which forage in the flowers of monoecious Ecballium elaterium (L.) A. Rich (Cucurbitaceae) were compared. The female flowers of E. elaterium resemble male flowers visually but are nectarless, and their number is relatively smaller. Apis mellifera was found to discriminate between the two genders and to pay relatively fewer visits to female flowers (mean of 30% relative to male flowers) from the beginning of their activity in the morning. The time spent by honeybees in female flowers is very short compared to that spent in male flowers. It is surmised that the bees remember the differences between the flowers where they foraged on the previous days. In contrast, the two species of solitary bees Lasioglossum politum (Morawitz) (Halictidae) and Ceratina mandibularis Fiese (Anthophoridae) visit the female flowers with nearly equal frequencies at the beginning of each foraging day and stay longer in these flowers. Over the day there is a decline in the relative frequency of visits to female flowers and also in the mean time spent in them. The study shows that bees can collect rewards at high efficiency from the flowers of Ecballium elaterium because of their partial discrimination ability and the scarcity of the mimic flowers. It is suggested that the memory pattern of some solitary bees may be different from that of Apis mellifera. It seems that the limited memory and discrimination ability of bees can lead to a high frequency of visits to the mimic flowers during a long flowering season.     

Anthecology ofSchrankia nuttallii (Mimosaceae) on the tallgrass prairie

Schrankia nuttalii flowers through late spring on the tallgrass prairie. Although each stem produces an average of 26 capitate inflorescences only 12% of those inflorescences will open each day to disperse and receive polyads. Each inflorescence may live up to 48 hours but anthers abscise by late afternoon on the first day and the filaments change color and lose their scent. The 78–93 florets comprising each inflorescence open synchronously before dawn or during early morning hours. First day inflorescences ofS. nuttallii are herkogamous and fragrant. They are nectarless. Bombyliid flies and male bees are infrequent floral foragers so the major pollinators include female bees representing five families;Anthophoridae, Apidae, Colletidae, Halictidae, andMegachilidae. All foraging insects ignore second day inflorescences although stigmas are still receptive. Although 97% of all bees collected onS. nuttallii carrySchrankia polyads in their scopae or corbiculae 59% also carry the pollen/pollinaria of one or more coblooming angiosperms. At least 98% of all bees carrying mixed pollen loads incorporate the pollen/pollinaria of one or more nectariferous taxa (e.g.Asclepias spp.,Asteraceae, Convolvulaceae, Delphinium spec., etc.). Species of halictid bees are more likely to carry pure loads ofS. nuttallii polyads (70%) than bees of the four remaining families. Due to the nectarless florets and high degree of polylectic foraging bee-pollination inS. nuttallii converges more closely with the pollination systems of some AustralianAcacia spp. than with most other xeric/tropical genera of mimosoids studied in the western hemisphere.     

Bee-pollination inHibbertia fasciculata (Dilleniaceae)

In direct contrast to mostHibbertia spp., the flowers ofH. fasciculata R. Br. ex D. C. bear only a single whorl of stamens and these stamens are arranged separately (not in typical bundles). The short filaments are appressed to the three carpels so that the inflated, porose and introrsive anthers form a centralized cluster obscuring the three ovaries. The three slender styles emerge at right angles from between the filaments. These styles curve upward and the stigmas form the three points of a triangle; each stigma is approximately one millimeter outside the centralized cluster of anthers. The flowers are nectarless and bear a bright yellow corolla. A pungent and unpleasant fragrance appears to be concentrated within the pollenkitt. When native bees attempt to forage for the pollen, within the cluster of anthers, the ventrally deposited loads of pollen, on the bees' abdomens, contact the outer triangle of stigmas. The major pollinators ofH. fasciculata are female bees in the polylectic genera,Lasioglossum (subgenusChilalictus, Halictidae) andLeioproctus (Colletidae). These bees carry an average of more than two pollen taxa when they are caught foraging onH. fasciculata. 78% of the 47 bees, captured onH. fasciculata carried the pollen from at least one sympatric taxon bearing nectariferous flowers (e.g., genera in theMyrtaceae, Compositae, andEpacridaceae). The pollination biology ofH. fasciculata is assessed in relation to the known radiation of bee-pollinated flowers in the genusHibbertia, and within theDilleniaceae s. l.     

Notes on the pollination mechanisms ofMoraea inclinata andM. brevistyla (Iridaceae)

Individual flowers ofMoraea inclinata are nectariferous and last about six hours. They appear to be pollinated largely by bees in the familyHalictidae (Lasioglossum spp.,Nomia spp.,Zonalictus) and to a lesser extent by bees in the familyAnthophoridae (Amegilla). The mechanism of bee-pollination inM. inclinata is the Iris type; i.e., each flower consists of three pollination units (an outer tepal, a partly exserted anther, and the opposed style branch which terminates in a pair of petal-like crests). Bees rarely visit more than one pollination unit per flower. Transferral of pollen to the bee is passive and nototribic although all bees collected on the flowers were female and 55% of the bees carried pollen loads with 2–5 pollen taxa in their scopae.Moraea brevistyla flowers are nectariferous but lack scent and last two days. They are visited infrequently by bees and only one femaleLasioglossum spec. carried the pollen ofM. brevistyla. Unlike flowers ofM. inclinata those ofM. brevistyla deposit pollen only on the head and thorax. Bee-mediated autogamy in both species is avoided due to the erratic foraging patterns of the bees and the flexibility of each stigma lobe as the bee backs out of the flower. Approximately 2–4 flowers in the inflorescences of both species (6–8 flowers/infloresence) develop into capsules.     

Fragrance analyses,an aid to taxonomic relationships of the genusCoryanthes (Orchidaceae)

All members of the investigated genusCoryanthes (subtribeStanhopeinae) are pollinated by male euglossine bees. The different fragrance profiles are the primary reproductive isolating mechanisms, because the flowers are interfertile. The fragrance patterns of 17 species ofCoryanthes were analyzed by gas chromatography as a means to improve the classification of this genus. A first amine (2-N-methylaminobenzaldehyde) was found to be the main fragrance compound of an as yet unclassifiedCoryanthes species.     

An ancient pollinator of a contemporary plant (Cyclamen persicum): When pollination syndromes break down

Pollination of Cyclamen persicum (Primulaceae) was studied in two wild populations in Israel. Buzz-pollination proved to be extremely rare, and performed by a large Anthophora bee only. The most frequent pollinators were various unspecialized species of thrips (Thysanoptera) and hoverflies (Syrphidae). In the Winter-flowering populations the commonest visitor was a small primitive moth, Micropteris elegans (Micropterigidae, Lepidoptera). These moths feed on pollen, copulate and oviposit within the flowers. From the rarity of buzz-pollination it is concluded that the genus Cyclamen co-evolved with large bees capable of buzz-pollination, but lost its original pollinators for unknown historical reasons. The vacant niche was then open to various unspecialized pollen consumers such as thrips, hoverflies and small solitary bees. While these insects are not specific to C. persicum and seem to play a minor role only, the moth strictly relies upon Cyclamen and seems to be the most efficient pollinator.     

Reward partitioning in Capparis spp. along ecological gradient

Summary The genus Capparis is represented in Israel by three taxons of the section spinosa. The pollinators of the three taxa are hawkmoths, crepuscular bees of the genus Proxylocopa and various daily bees. However, the efficiency of the different pollinators is very varied with respect to the individual taxons. Hawkmoths were frequently observed as pollinators of C. spinosa var. aravensis and C. ovata, but rarely on C. spinosa var. aegyptia. All the other bees, on the other hand, were found abundantly on all three taxons, all over the country. The three taxa all provide different rewards for their particular pollinators. Bees visiting C. spinosa var. aegyptia are provided with a lot of pollen but a relatively small amount of nectar, with a low sugar content. C. spinosa var. aravensis and C. ovata (the flowers visited more by hawkmoths), have less pollen but a higher amount of nectar which has a higher concentration of sugar. In drier habitats the emphasis of the reward provided by the flowers is nectar, whilst in the Mediterranean habitats it is the pollen which is the reward, without any connection to the systematic origin of the plant.     

Solitary invasive orchid bee outperforms co-occurring native bees to promote fruit set of an invasive Solanum

Our understanding of the effects of introduced invasive pollinators on plants has been exclusively drawn from studies on introduced social bees. One might expect, however, that the impacts of introduced solitary bees, with much lower population densities and fewer foragers, would be small. Yet little is known about the potential effects of naturalized solitary bees on the environment. We took advantage of the recent naturalization of an orchid bee, Euglossa viridissima, in southern Florida to study the effects of this solitary bee on reproduction of Solanum torvum, an invasive shrub. Flowers of S. torvum require specialized buzz pollination. Through timed floral visitor watches and two pollination treatments (control and pollen supplementation) at three forest edge and three open area sites, we found that the fruit set of S. torvum was pollen limited at the open sites where the native bees dominate, but was not pollen limited at the forest sites where the invasive orchid bees dominate. The orchid bee’s pollination efficiency was nearly double that of the native halictid bees, and was also slightly higher than that of the native carpenter bee. Experiments using small and large mesh cages (to deny or allow E. viridissima access, respectively) at one forest site indicated that when the orchid bee was excluded, the flowers set one-quarter as many fruit as when the bee was allowed access. The orchid bee was the most important pollinator of the weed at the forest sites, which could pose additional challenges to the management of this weed in the fragmented, endangered tropical hardwood forests in the region. This specialized invasive mutualism may promote populations of both the orchid bee and this noxious weed. Invasive solitary bees, particularly species that are specialized pollinators, appear to have more importance than has previously been recognized. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Floral mimesis inThelymitra nuda (Orchidaceae)

Insect pollination occurred inThelymitra nuda R. Br. on sunny days when the ambient temperature exceeded 20 °C. The flower buds on a raceme opened subsynchronously displaying the brightly-colored, actinomorphic perianth and exposed the contrastingly-colored, scented and ornamented column. InT. nuda the staminodes and the filament of the fertile stamen are fused to one another producing an inflated hood over the anther. This staminodal hood is terminated in two non-ornamental, but brightly-colored, central lobes and two terete lateral lobes bearing approximately 400 white trichomes. Each trichome bears a double chain of 30–40 spherical, rugulose cells. Female bees, in the genusLasioglossum (Halictidae), were observed to land directly on the hood and curled their bodies around the four lobed tip of the staminodal complex. The bees attempted to forage on the lobes as if they were collecting pollen from fertile, poricidal stamens. These bees applied thoracic vibration to the yellowish central lobes and actively scraped the trichome clusters (Pseudopollen) with their forelegs. Bees carried the pollinaria ofT. nuda dorsally on their abdomens. Abdominal contact with the rostellum appeared to occur when the female bee disengaged herself from the staminodal hood. Observations made of bees on co-blooming flowers, and analyses of pollen loads collected by bees suggested that the orchid flower mimics the guild of blue-purple flowers that lack floral nectar but offer pollen in poricidal anthers. The models ofT. nuda are co-bloomingLiliaceae in the generaDichopogon andThysanotus. However, nectarless, buzz-pollinated flowers are also extensively distributed over the orchid’s range. More than 30% of the flowers in theT. nuda population had their pollinaria removed, suggesting a high capacity for cross-pollination in an orchid genus usually considered to be self-pollinated via mechanical autogamy. This study confirmed previous predictions that column modifications represented a trend towards pseudanthery.     

Pollination ofOpuntia lindheimeri and related species

The large, yellow, bowl-shaped flowers ofOpuntia lindheimeri, O. discata, O. phaeacantha major, andO. compressa in Texas are visited by various species of beetles and bees. The beetles and small bees (Perdita, Dialictus) are pollen thieves. The pollinators are the medium-sized and larger bees (Melissodes, Diadasia, Lithurge, Megachile, Agapostemon, etc.). Different species of theOpuntia lindheimeri group have the same pollination system and there is no evidence of any floral isolation between them. The pollination system of these species ofOpuntia in Texas is essentially the same as that ofEchinocereus fasciculatus andFerocactus wislizeni in Arizona.Pollination of North American Cacti, II.—SeeGrant & Grant (1979).     

Stamen movements in flowers ofOpuntia (Cactaceae) favour oligolectic pollinators

Opuntia brunneogemmia andO. viridirubra occur sympatrically in the Serra do Sudeste, Rio Grande do Sul, Brazil. Their flowers have 450–600 thigmonastic stamens and provide large amounts of pollen and nectar for bees. Bees of 41 species were registered at the flowers ofO. brunneogemmia and 30 at the flowers ofO. viridirubra. Females of three oligolectic species are the only effective pollinators:Ptilothrix fructifera (Anthophoridae),Lithurgus rufiventris (Megachilidae), andCephalocolletes rugata (Colletidae). During their visits inOpuntia-flowers, bees touch the filaments and stimulate the movement of the stamens to the centre of the flower. At the end of this movement, the anthers are densely packed around the style. As a consequence the pollen is presented in an easily accessible upper layer of anthers and various, nearly inaccessible lower layers. The lower layers contain about 80% of the pollen reward. Only females of the three oligolectic pollinators exploit the pollen from the lower layers and reach the nectar furrow. Therefore, through their stamen movements,Opuntia flowers hide most of their pollen from flower visitors but favour effectively pollinating, oligolectic bees.     

Floral constancy in bumble bees: handling efficiency or perceptual conditioning?

Individual bees often prefer flowers of the same species that they are already foraging on, and other individual bees prefer other flowers. This floral constancy has classically been explained as a learned behavior by which bees avoid wasting time switching between handling techniques. Choice trails were given to Bombus vagans workers that were freely foraging in mixed and pure fields of Trifolium pratense, T. repens, Viccia cracca, and Prunella vulgaris. Contrary to expectation, (1) bees showed if anything a stronger preference for their flower type in pure fields where they lacked experience than in a mixed field where they had had the opportunity to learn, (2) there was greater constancy in a mixed field of the two morphologically similar Trifolium species than in a mixed field of the morphologically disparate T. pratense and P. vulgaris, and (3) bees were more willing to switch between flowers of distinct morphologies when the colors were similar than between flowers of distinct colors when the morphologies were similar. We suggest that constancy is due to some form of perceptual conditioning whereby individual bees become temporarily sensitized to one or a few floral cues.     

Bees assess pollen returns while sonicating Solanum flowers

Summary Can bees accurately gauge accumulating bodily pollen as they harvest pollen from flowers? Several recent reports conclude that bees fail to assess pollen harvest rates when foraging for nectar and pollen. A native nightshade (Solanum elaeagnifolium Cavanilles) that is visited exclusively for pollen by both solitary and social bees (eg. Ptiloglossa and Bombus) was studied in SE Arizona and SW New Mexico. The flowers have no nectaries. Two experiments were deployed that eliminated pollen feedback to the bees by experimentally manipulating flowers prior to bee visits. The two methods were 1) plugging poricidal anthers with glue and 2) emptying anthers of pollen by vibration prior to bee visitation. Both experiments demonstrated that bees directly assess pollen harvest on a flower-by-flower basis, and significantly tailor their handling times, number of vibratile buzzes per flower and grooming bouts according to the ongoing harvest on a given flower. In comparison to experimental flowers, floral handling times were extended for both Bombus and Ptiloglossa on virgin flowers. Greater numbers of intrafloral buzzes and numbers of times bees groomed pollen and packed it into their scopae while still on the flower were also more frequent at virgin versus experimental flowers. Flowers with glued andreocia received uniformly brief visits from Bombus and Ptiloglossa with fewer sonications and virtually no bouts of grooming. Curtailed handling with few buzzes and grooms also characterized visits to our manually harvested flowers wherein pollen was artificially depleted. Sonicating bees respond positively to pollen-feedback while harvesting from individual flowers, and therefore we expect them to adjust their harvesting tempo according to the currency of available pollen (standing crop) within Solanum floral patches.     

Behavioral responses by bumble bees to variation in pollen availability

Summary Pollen-collecting bumble bees (Bombus spp.) detect differences between individual flowers in pollen availability and alter their behavior to capitalize on rewarding flowers. Specific responses by bees to increased pollen availability included: longer visits to flowers; visits to more flowers within an inflorescence, including an increased frequency of revisits; an increased likelihood of grooming while the bee flow between flowers within the inflorescence; and more protracted inter-flower flights, probably because of longer grooming bouts. The particular suite of responses that a bee adopted depended on the pollen-dispensing mechanism of the plant species involved. Bees buzzed previously-unvisited Dode-catheon flowers longer than empty flowers. In contrast, pollen availability did not significantly affect the duration of visits to Lupinus flowers, which control the amount of pollen that can be removed during a single visit. Simulation results indicate that the observed movement patterns of bumble bees on Lupinus inflorescences would return the most pollen per unit of expended energy. The increased foraging efficiency resulting from facultative responses by bees to variation in pollen availability, especially changes in the frequency and intensity of grooming, could correspondingly decrease pollen dispersal between plants.     

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.