Oil-collecting Bees Research Articles

Description of the male of Rediviva steineri Kuhlmann, 2012 (Hymenoptera: Melittidae), an endemic oil-collecting bee species from South Africa

We describe the male of Rediviva steineri Kuhlmann, 2012; distinguished by the shape and the margin of the apical plate of the eighth sterna and the vestiture of metasomal terga two and three. Five males were collected at the type locality of the female (Farm Doornbosch, Western Cape, South Africa). We examined the types of three other closely related species (R. pallidula, R. brunnea and R. whiteheadi) and provide images of the eighth sterna for comparison with R. steineri and update Whitehead et al.’s (2008) identification key for the males of these species.

Description of a new species within the Satyrium longicauda (Orchidaceae) complex from South Africa, based on integrative taxonomy

Although delimitations of plant species are traditionally based on the study of herbarium specimens, new species can also be identified using multiple lines of evidence (integrative taxonomy). An integrative approach was implemented to identify a new species of the orchid genus Satyrium from the Midlands area of KwaZulu-Natal, South Africa, described here as S. cernuum. This species shares an overall similar floral morphology with five other sympatric morphotypes within the S. longicauda complex reported from the type locality but can be diagnosed by a combination of vegetative and floral traits and flowering phenology. According to a published phylogeny based on DNA sequences, the new species forms a monophyletic clade that is nested within S. longicauda and is supported as sister to the other S. longicauda morphotype that is uniquely characterised by a single erect leaf. The new species differs from this morphotype by the orientation of its flowers which are obtuse (vs. right-angled) relative to the inflorescence stem, spreading (vs. spreading to recurved) sepals, relatively short (vs. long) spurs that lack nectar and by its production of elevated levels of diacetin, a fatty-acid derived compound. Other S. longicauda morphotypes differ in the number and position of their leaves and a later flowering period. In addition, the new species is exclusively pollinated diurnally by the oil-collecting bee species Rediviva neliana, rather than being pollinated nocturnally by settling moths and hawkmoths; it is thus reproductively isolated from sympatric morphotypes. The formal recognition of the new species, which is known from two adjacent populations in an area of occupancy ≤1 km2 makes it a matter of immediate conservation concern. An identification key to the morphotypes of the S. longicauda complex from KwaZulu-Natal, including the newly described species, is provided. This study shows the value of using integrative taxonomy in the South African flora for the recognition of recently diverged taxa.

Floral oil production in a family dominated by pollen flowers: The case of Macairea radula (Melastomataceae)

The Melastomataceae family, the largest radiation of pollen flowers, has been reported to offer floral oils exclusively in the Olisbeoideae subfamily. However, species from other clades such as Macairea radula (Marcetieae, Melastomatoideae) exhibit staminal glands that secrete oil-like viscous substances whose chemical composition and function are still unknown. We used anatomical sections and histochemical tests to characterize these staminal glands and their exudate. We also used GC–MS to characterize the chemical composition of the oil from the flowers and the scopae of visiting oil bees (Centris aenea). The staminal glands consist of glandular emergences with a multiseriate stalk and a conspicuous multicellular secretory head. Histochemical tests revealed the presence of lipids and phenolic compounds inside the glandular head cells. Although histologically different from trichomes, these glands are morphologically similar to trichomatic elaiophores. GC–MS confirmed the non-volatile lipidic nature of the staminal gland secretion, which consists of a mix of medium to long chain alkanes and nutritious fatty acids. Therefore, M. radula staminal glands produce oils similar in composition to the oils produced as bee reward by other angiosperm flowers. Some of these compounds were also found in the oils extracted from visiting bee scopae, suggesting that the oils produced by the staminal glands can be collected by bees. In addition, or alternatively, these oils could promote better adhesion of pollen to the bee's body. Oil production by staminal glands of M. radula may attract oil-collecting bees more consistently, ultimately contributing to the plants’ reproductive success.

Pollinator Community Predicts Trait Matching between Oil-Producing Flowers and a Guild of Oil-Collecting Bees.

AbstractThe impact of pollinator community diversity on trait matching in plant-pollinator interactions is poorly studied, even though many mutualisms involve multiple interaction partners. We studied 10 communities in which one to three species of oil-collecting Rediviva bees pollinate the long-spurred, oil-producing flowers of Diascia "floribunda" to examine how pollinator diversity affects covariation of functional traits across sites and trait matching within sites. Floral spur length was significantly correlated with weighted grand mean foreleg length of the local bee community but not with foreleg length of individual bee species. The closeness of trait matching varied among populations and was inversely related to pollinator community diversity. For all bee species, trait matching was closest at sites characterized by exclusive pairwise interactions. Reduced trait matching associated with increased community diversity for individual pollinator species but close matching at the community level supports the importance of community context for shaping interacting traits of flowers and pollinators.

Vanillaflowers: much more than food-deception

AbstractIn many flowering plants the attraction of pollinators is related to some kind of deception. Pollination by food-deception occurs in several angiosperm groups and is particularly widespread in orchids. Despite the apparent evolutionary success of pollination by food-deception, food-deceptive orchids show a low level of fruit set. Although studies are scarce, the pollination of Vanilla has been usually associated with nectar-deception. In Vanilla spp. (Vanilla bahiana, V. bicolor, V. chamissonis, V. edwallii, V. hartii, V. phaeantha, V. paulista, V. planifolia, V. ribeiroi and V. pompona), understanding the factors associated with pollinators is essential, since in vanilla production a cumbersome process of supplementary manual pollination is necessary to increase fruit set, which is frequently low under natural conditions. The production of floral rewards was investigated here in ten Neotropical Vanilla spp. based on morpho-anatomy and histochemical analyses of flowers. Six species (Vanilla bahiana, Vanilla bicolor, Vanilla chamissonis, Vanilla hartii, Vanilla phaeantha and Vanilla pompona) offer nectar as a reward. In Vanilla ribeiroi, the long trichomes of the labellum base are rich in starch grains and proteins, characteristic of food-hairs. The only secretory structures of Vanilla edwallii are osmophores on the inner surface of the labellum that are related to the attraction of oil-collecting bees as pollinators. Vanilla spp. possess sepaline and labellar osmophores. Inside the labellum the osmophores are arranged along longitudinal lines and act as resource guides. Although it is widely known that Vanilla flowers attract pollinators by nectar deception, the present data reveal that there may be a lack of knowledge regarding pollination in this group since the offer of nectar appears to be a common condition, at least for the euglossine-pollinated Neotropical clade. The remaining Neotropical groups exhibit other pollination strategies, such as the production of food-hairs and fragrances that attract oil-collecting bees to the flowers. The study of Vanilla pollination is extremely important because the need for manual pollination, added to the ripening and curing time, causes vanilla to be one of the most expensive spices in the world. According to the data presented here, the pollination systems of vanilla are much more diverse than classical “food deception”.

Structural diversity of elaiophores in Argentine species of Malpighiaceae: morphology, anatomy, and interaction with pollinators.

Most Neotropical Malpighiaceae species are characterized by having zygomorphic flowers and oil glands in the sepals called elaiophores; these floral characteristics are associated with a particular pollination syndrome through oil-collecting bees. This work proposes a study about the structural characteristics of elaiophores in 18 species of Malpighiaceae present in Argentina. The main objectives are to describe the morphology and anatomy of the elaiophores, to detect variation in the number of glands, to compare similarities or differences in elaiophores of species belonging to different lineages, and to know about the potential pollinators and their association with the structural traits of the elaiophores. The morphology and the anatomy were studied using traditional methods of scanning electron and bright-field microscopes. Field trips were carried out to capture oil-collecting bee species on flowers, in different natural populations. Different measurements were taken in the flowers, elaiophores, and oil-collecting bees and were statistically analyzed. Although elaiophores showed a common pattern, some particularities in number, morphology, and anatomy were detected; few of these seem to be restricted to some groups of species phylogenetically related. As regards pollinators, a positive tendency was observed between the size of the flowers, elaiophores, and oil-collecting bees. However, the thickness of the cuticle presented a negative association with the size of the elaiophore and consequently with the floral diameter, which could be presumably related to the foraging behavior and/or the structure of oil-collecting apparatus of the bee species.

Teasing out the functional groups of oil-collecting bees in the light of the pollination of Nierembergia flowers

Teasing out the functional groups of oil-collecting bees in the light of the pollination of Nierembergia flowers

Relicthemisia, a new subgenus of the oil-collecting bee genus Centris Fabricius, 1804 with notes on distribution and host plants of C. xanthomelaena Moure & Castro, 2001 (Hymenoptera: Apidae)

Centris xanthomelaena Moure & Castro, 2001 is a relict species, endemic to northeastern Brazil and broadly recorded within the semiarid region of Caatinga xerophilous open vegetation. It was originally included in the subgenus Paracentris Cameron, 1903 but posteriorly interpreted as remotely related to it or to the subgenus Centris s. str. Fabricius, 1804. In this paper it is proposed to recognize this species as the single member of the monotypic Relicthemisia, a new subgenus which belongs to the ‘Centris group’, one of the main internal lineages of the genus. The proposition of this new subgenus is based on both, morphological and molecular data which indicate its long history as a distinct lineage. Distribution records, floral hosts as well as photographs of both sexes of C. xanthomelaena are also provided.

The first case of gynandromorphy in <i>Centris pallida</i> (Hymenoptera: Apidae: Centridini)

A case of gynandromorphy is reported for the first time for Centris pallida Fox, a bee species found predominantly in the deserts of the southwestern United States and northern Mexico. This specimen marks only the second report of a gynandromorph within the tribe of oil-collecting bees, Centridini, and the first Centris Fabricius. The specimen exhibits mosaic gynandromorphy, with male and female characteristics randomly distributed throughout the body. Males of C. pallida are morphologically and behaviorally dimorphic (a large and a small male morph), and the male characteristics of the gynandromorph are more similar to the large male morph, which is also most similar in head width to the specimen.

Assessment of interactions between oil flowers and floral visitors in world biomes

Abstract Specialized glands that produce and store floral oil are found in 11 families of flowering plants, with greater representation in Malpighiaceae. Solitary bees use this resource to feed larvae and for cell lining. Oil interactions have been reported mainly at the population level and in some community studies that have commonly ignored not only the fewer representative families of oil-offering flowers, but also the floral visitors that do not collect floral oil. We have compiled and examined the interactions between oil-offering flowers and floral visitors in world biomes, to describe the structural patterns of the oil interaction meta-network and evaluate the species' functional roles. We reviewed 169 studies, which mainly used a phytocentric approach, reporting 1460 interactions between 214 species of oil-offering flowers and 377 species of floral visitors. Malpighiaceae and bees (mainly oil-collecting bees) were the most frequently investigated. The meta-network of oil interactions showed a modular structure, mainly influenced by botanical families, and core–periphery organization. The most important functional roles were associated with Malpighiaceae and oil-collecting bees, possibly due to their representativeness and geographic distribution.

Rediscovery of the Rare Bee Epeoloides pilosulus in Manitoba (Hymenoptera: Apidae)

Epeoloides pilosulus (Cresson) (Hymenoptera: Apidae) is an exceptionally rare bee of conservation concern. Epeoloides are cleptoparasites of the oil-collecting bees Macropis (Hymenoptera: Melittidae), which specialize on oil-producing species in the genus Lysimachia (Ericales: Primulaceae). We report on the first records of E. pilosulus in Manitoba in 95-years, and only the fifth through eighth specimens for Canada since 1960. Manitoban records of Macropis are also provided.

Where could Centris nigrescens (Hymenoptera: Apidae) go under climate change?

Climate change (CC) is an important driver affecting pollination and pollinators. This paper aims to provide an updated potential distribution for Centris nigrescens Lepeletier, 1841, and infer CC effects upon it. We used ten modeling methods to infer the potential distribution of C. nigrescens. We measured the extent of species’ suitable area (SSA) that is and maybe within protected areas and biogeographical provinces in both current and future scenarios. C. nigrescens seems to be restricted to the Tropical Region in the Americas. Geographical barriers affecting the species’ distribution are the Andean Cordillera and the Caribbean Sea. We recorded the species for the first time in Panama. In the future, SSA is expected to increase about 36% but with a partial reduction in both Amazon forest and South American savannas. Also, the SSA’ within protected areas would decrease by 1.3%. Considering the species’ range shifts under CC, it will be important to explore if the fragmentation of the suitable areas of the species’ range pattern in both Amazon forest and South American savannas will be the same as for other oil-collecting bees. It will also be essential to explore possible consequences on oil-producing plants' pollination in those areas.

Two new species of oil-collecting bees of Centris (Melanocentris) from Colombia (Hymenoptera: Apidae)

ABSTRACT In this article are described two new species of oil-collecting bees of Centris (Melanocentris) from Colombia. Centris (Melanocentris) marinae sp. nov. occurs in the northeast, César Department, while C. (Melanocentris) germani sp. nov. occurs in the southeast, in the Caquetá, Meta and Vaupés Departments, as well as in the Amazonas State in northwestern Brazil. Photographs of both new species and a distribution map are also presented.

The role of ontogenetic allometry and nonallometric flower shape variation in species-level adaptive diversification - Calceolaria polyrhiza (Calceolariaceae) as a case study.

Organism shape changes predictably during ontogeny, resulting in specific patterns of ontogenetic allometry. In several plant and animal lineages, among-species variation in the shape of mature organisms mirrors variation along their growth trajectories. Hence, ontogenetic allometry is an important bias in evolution. This bias should be stronger at reduced evolutionary time scales, in which among-trait correlations had less time to evolve. Nevertheless, it was shown that adaptation of organism shape frequently involved departures from the ancestral ontogenetic allometry. Moreover, only a moderate fraction of shape variation is correlated with size during ontogeny. Hence, nonallometric variation in shape (NAVSh) is likely to contribute to adaptation, even at reduced evolutionary time scales. We explored the contributions of allometric variation in shape (AVSh), NAVSh, and size variation to adaptive evolution in the angiosperm species Calceolaria polyrhiza. This strongly relies on oil-collecting bees for pollination and experienced transitions in the size of pollinators during the last 2 Ma. Using geometric morphometrics, we described corolla morphology in several populations across its distribution range. Variation in corolla shape was decomposed into an allometric and a nonallometric component, and corolla size was estimated. We then looked for the correlation between these aspects of morphology and the pollinator. Our results suggest that adaptation to pollinators with different sizes relied on NAVSh, which resulted from shifts in the allometric slope and from shape changes that occurred early in flower development. We conclude that NAVSh can contribute to adaptation in flowering plants, even at the species-level.

Food Reward Chemistry Explains a Novel Pollinator Shift and Vestigialization of Long Floral Spurs in an Orchid

During the evolutionary history of flowering plants, transitions between pollinator groups (pollinator shifts) have been frequent,1 and contributed to the spectacular radiation of angiosperms.2 Although the evolution of floral traits during pollinator shifts has been studied in real time under controlled laboratory conditions,3 it is challenging to study in nature and therefore poorly understood.4-7 Using a comparative, multidisciplinary approach, we dissect the evolution of floral traits during a pollinator shift in the long-spurred African orchid Satyrium longicauda. Phylogenetic analysis and ecological experiments revealed a shift from moth- to oil-collecting bee pollination. Remarkably, flowers of the bee-pollinated form are similar in morphology, color, and overall volatile chemistry to those of moth-pollinated forms, but differ in having spurs that are mostly devoid of nectar, and have an elevated presence of the oil-derived compound diacetin, which oil-collecting bees use as a cue for oil presence.8 Experiments demonstrated that long spurs are critical for pollination of a moth-pollinated form, but are not needed for pollination of the bee-pollinated form. We conclude that the pollinator shift in Satyrium was mediated by a switch in chemistry of the pollinator reward. The ancestral presence of diacetin might have served as a pre-adaptation for bee pollination, whereas the current mismatch between flower morphology and bees is due to the retention of vestigial floral spurs. These results elucidate the sequence of floral evolution in the early stages of pollinator shifts and help to explain the assembly of suites of co-varying traits through pre-adaptation and vestigialization.9-12.

Different Pollinators' Functional Traits Can Explain Pollen Load in Two Solitary Oil-Collecting Bees.

Simple SummaryPollinators’ features, especially those with a functional role during the pollination process, have been shown to be a good predictor of pollen load for some bee species, but little is known about solitary bees. Here, I have used two solitary oil-collecting bees to understand the impact of functional pollinator traits on the pollen load of two oil-secreting Calceolaria herb species. I therefore measured the visitation frequency, the time spent manipulating the flower and the body size and pollen load for each bee species. The results reveal that each pollinator species visits different Calceolaria species (C. cavanillesii and C. filicaulis) for pollen and/or oil and a few other herb species for pollen collection. In addition, each bee species showed different features involved in Calceolaria pollen collection and load. In the case of C. chilensis, only its body size affected its pollen load, while in C. subcaeruleus, both its body size and the time spent manipulating the flower affected the total pollen that this bee was able to carry. These results highlight the role of pollinators’ functional traits at different stages of the pollination process, specifically during pollen collection and transport, and even more in specialized plant-pollination systems.Functional traits have been shown to be a good predictor of pollen load for some pollinator bee species, but little is known about solitary bees. In this study, I used two solitary oil-collecting bees to explore the impact of functional traits on the pollen load of two oil-secreting Calceolaria species. I therefore measured the visitation frequency, the time spent manipulating the flower, pollinator body size and pollen load for each bee species. The results reveal that each pollinator visits different Calceolaria species (C. cavanillesii and C. filicaulis) for pollen and/or oil and at least another four herb species for pollen in different proportions. In addition, each bee species presents different functional traits that affect Calceolaria pollen load. For C. chilensis, it was only its body size that affected the Calceolaria pollen load, while in C. subcaeruleus, both body size and handling time together account for its pollen load. Overall, these results highlight the role of pollinators’ functional traits in different stages of the pollination process, and even more in specialized plant-pollination systems.

Nesting behavior of the oil-collecting bee Epicharis (Triepicharis) analis Lepeletier (Hymenoptera: Apidae) in an urban area of Rio de Janeiro, RJ, Brazil

An aggregation of the oil-collecting bee Epicharis (Triepicharis) analis Lepeletier was studied at the Jardim Botânico do Rio de Janeiro, Brazil. The nesting area occupied 609 m2 of mostly sandy flat soil. The nest architecture was relatively simple, with a main tunnel of approximately 45 cm in depth with two to five lateral tunnels ending in a single brood cell. The entrance remained open, but not always directly exposed. Adult activity lasted approximately 75 days. The females dug the tunnels, constructed the brood cells, collected provisions and laid the eggs in about three days. Diapause occurred in the postdefecating larval stage, and there was no cocoon. The cleptoparasitic apid bees Rhathymus unicolor (Smith) and Mesoplia rufipes (Perty) were registered attacking the nests. Nest architecture and the morphology of the brood cells are described and illustrated.

Community-level plant–pollinator interactions in a Palaeotropical montane evergreen oak forest ecosystem

ABSTRACT The montane terrain of northern Laos is covered by species-rich subtropical evergreen oak forests, home to endemic tree genera such as Mytilaria (Hamamelidaceae), and characterised by the coexistence of several honeybee and bumblebee species. We explored community-level plant–pollinator interactions of this unique little-known ecosystem. Extensive direct observations on flowering phenology and flower-visitor assemblages of 288 plant species of 82 families were conducted in a montane forest ecosystem in Houaphanh and Xiangkhouang Provinces, Laos, from 2005 until 2016. Based mainly on the extensive flower-visit data, we assessed the pollination system of each plant species. Five sympatric honeybee species (Apis dorsata, A. laboriosa, A. cerana, A. florea and A. andreniformis) were common on various types of flowers, and floral preferences differed among species. Long-tongued bees belonging to Bombini and Anthophorini (Apidae) were species-rich and frequent visitors on various deep flowers, especially Acanthaceae, Balsaminaceae, Lamiaceae, Rubiaceae and Zingiberaceae. Character displacement by tongue length was observed among the bee species, and many relaxed species-specific and species-semispecific interactions were observed between the bees and the deep-flowers. Four plant species, in the genera Mytilaria, Chloranthus, Dioscorea and Cryptocarya, were visited exclusively by thrips. Two plant species, in the genera Lysimachia and Thladiantha, had oil-secreting flowers, which were specifically visited by the oil-collecting bees Macropis and Ctenoplectra, respectively. The dominant pollination system assessed was general insect pollination (31%), followed by long-tongued bee, small bee, honeybee, dipteran, lepidopteran, beetle, wasp, carpenter bee, thrips (e.g. the endemic genus Mytilaria), bird and hemipteran pollination. Our results suggest that the plant–pollinator interactions in the Palaeotropic montane ecosystem are characterised by significant contribution of the five honeybee species and species-rich, morphologically diverse long-tongued bees, both of which have contributed to shaping the remarkable diversity of angiosperms with deep flowers.

Notas sobre la arquitectura del nido de Centris (Centris) caxiensis Ducke (Hymenoptera: Apidae) en un fragmento urbano de bosque seco en el noreste de Brasil

We described the nest architecture and the brood cell morphology of the oil-collecting bee Centris caxiensis . The nest is a single and unbranched tunnel measuring between 37 and 49 cm in length slant obliquely into the ground. There were one or two brood cells at the end of the gallery oriented vertically. The brood cells are urn-shaped with a plug containing a central hollow process. The nest morphology and the brood cells followed a similar pattern to the other ones reported for species of the subgenus Centris s. str.

A Nesting Aggregation of Rediviva intermixta (Melittinae: Melittidae) with Males Sleeping Together in Burrows: Namaqualand, South Africa

A nest aggregation of the oil-collecting bee Rediviva intermixta (Cockerell, 1934) (Hymenoptera: Melittidae: Melittinae) was found associated with a mound of harvester termite, Microhodotermes viator (Latreille, 1804) occupying a clay-rich bank. We first noticed this nest aggregation by the intensive patrolling of seemingly hundreds of males searching for females close to the ground. We estimate the density of nests as 194 nests/m2 or 2917 nests in the 15m2 aggregation. This short communication presents observations on the daily activity and interactive behavior of males and females at the nesting holes. We provide the first account for this family of the males sleeping together in burrows, rather than on flowers.