Oil-collecting Bees Research Articles

Difference in reproductive traits of two sympatric species of Stigmaphyllon (Malpighiaceae) throughout their distribution range: Are they context-dependent?

Populations of widely distributed plants may experience varying climatic or ecological conditions, leading to uneven evolution of reproductive traits. However, studies on reproductive biology usually focus on just one, or rarely two, sampling areas. In this study, we performed a geographical comparative analysis of the flowering pattern, pollination biology and breeding system of Stigmaphyllon bonariense and S. jatrophifolium (Malpighiaceae) throughout their natural distribution in Argentina, classifying them as ‘northern’ or ‘southern’ according to their geographic location. For this, we selected 4 populations for S. bonariense and 3 for S. jatrophifolium to characterized the flowering peak at both the individual (IFP) and population (PFP) levels, the floral display per inflorescence, the richness of Malpighiaceae species and their pollinators, and the stigmatic and body pollen loads of the pollinators. In addition, we performed manipulative experiments to determine the breeding system. Our results showed that the duration of flowering phenology and the floral display vary between northern and southern populations of both species. These traits include flowering duration and the number of flowers at anthesis per inflorescence (floral display). In addition, the pollination context exhibited latitudinal differences in species richness, phenology, body size of oil-collecting bees, and visitation frequency. Besides, the number of co-flowering Malpighiaceae species varied among populations. However, no considerable differences were observed among populations in terms of stigmatic and body pollen load in pollinators of both species. The breeding system was invariable and consistent in both species with self-incompatibility (SI). These findings suggest that certain reproductive traits of both Stigmaphyllon species are context-dependent and would allow the species maximise reproductive success in each population. Therefore, our results demonstrate that large-scale geographical studies (i.e., several populations with different climatic conditions) and the analysis of various phenological traits are necessary to better understand the reproductive biology of plant species.

Review of the genus Ctenoplectra Kirby (Apidae: Apinae: Ctenoplectrini) from India with two new country records

The oil-collecting bees of the genus Ctenoplectra Kirby from India are revised based on specimens deposited in the National Zoological Collection, Zoological Survey of India and University of Agriculture, GKVK, Bengaluru. The most exciting part of this revision is the addition of two Southeast Asian species of this genus, C. cornuta Gribodo and C. davidi Vachal, to the Indian fauna, which previously consisted of only C. chalybea Smith.

Nesting biology of two species of oil-collecting bees of the genus Paratetrapedia s.l. (Apidae: Tapinotaspidini) in Argentina

Nesting biology of two species of oil-collecting bees of the genus Paratetrapedia s.l. (Apidae: Tapinotaspidini) in Argentina

Pollinator-mediated selection on Krameria oil flowers: a flower-pollinator fit adaptation to an atypical oil-collecting behaviour?

Spatial variation in plant-pollinator interactions is a key driver of floral trait diversification. A so far overlooked qualitative aspect of this variation is the behavioural component on flowers that relates to the pollinator fit. We tested the hypothesis that variation in pollinator behaviour influences the geographical pattern of phenotypic selection across the distribution range of the oil-producing Krameria grandiflora (Krameriaceae). This variation mainly involves the presence or absence of flag petal grasping, which is only performed by representatives of Centris (Centridini, Apidae), an oil-collecting bee group highly associated with Krameriaceae pollination. We quantified variation in floral traits and fitness and estimated pollinator-mediated selection in five populations at a large geographical scale comprising the entire species range. In each population, we sampled individual pollen arrival and germination as a fitness measure, indicating pollination success and pollination performance, which was then relativized and regressed on standardized flower-pollinator fit (flag-stigma distance), advertisement (sepal length) and reward (oil volume) traits. This generated mean-scaled selection gradients used to calculate geographical selection dispersion. Unexpectedly, stronger selection was detected on the flower-pollinator fit trait in populations highly associated with the absence of flag petal grasping. Geographical variation in selection was mainly attributed to differential selection on the flag-stigma distance generating a selection mosaic. This may involve influences of a spatial variation in pollinator behaviour as well as composition and morphology. Our results show the adaptive significance of the specialized flag petals of Krameria in the absence of the grasping behaviour and highlight the contribution of geographical variation in pollinator behaviour on flowers in driving selection mosaics, with implications for floral evolution, adaptation to pollinator fit and phenotypic diversity in specialized systems.

Phenotypic selection patterns in a hybrid zone between two Calceolaria species with contrasting pollinators: insights from field surveys and fitness assessments.

Hybrid zones provide natural experimental settings to test hypotheses about species divergence. We concentrated on a hybrid swarm in which oil-collecting bees and flower-pecking birds act as pollinators of two Calceolaria species. We asked whether both pollinators contributed to flower divergence by differentially promoting prezygotic fitness at the phenotypic extremes that represent parentals. We studied pollinator-mediated selection on phenotypic traits critical in plant-pollinator mechanical interaction, namely plant height, reward-to-stigma distance, and flower shape. We utilised the quantity and quality of pollen deposited as fitness measures and distinguished between the contribution of the two pollinator types. Results showed uni- and bivariate disruptive selection for most traits through pollen grains deposited by both pollinators. Bird-mediated fitness favoured low plants with a long reward-to-stigma distance and a straight corolla, while bee-mediated fitness favoured tall plants with a short reward-to-stigma distance and curved corolla. In addition, stabilising selection at one end of the phenotypic range showed a bird-mediated reproductive asymmetry within the swarm. The disruptive pattern was countered, albeit weakly, by hybrids receiving higher-quality pollen on the stigmas. Results suggest that pollinator-mediated selection promotes divergence of integrated flower phenotypes mechanically adjusted either to bees or birds underscoring the importance of pollinator specialisation in diversification.

Taxonomic revision of the oil-collecting bee subgenus Epicharis (Epicharitides) Moure, 1945 (Hymenoptera: Apidae), with the description of two new species

A taxonomic revision of the oil-collecting bees of the subgenus Epicharis (Epicharitides) Moure, 1945 is provided. A total of nine species were recognized: E. cockerelli Friese, 1900; E. duckei Friese, 1901; E. iheringi Friese, 1899; E. luteocincta Moure & Seabra, 1959; E. minima (Friese, 1904); E. obscura Friese, 1899, and E. rufescens Moure & Seabra, 1959, along with E. mesoamericana sp. nov. and E. lia sp. nov., two new species from the Central American and Amazonian provinces, respectively. Redescriptions, diagnoses, and figures of specimens of both sexes, floral records, distribution maps, an identification key, and an updated catalogue of all species of the group are also provided. In addition, the lectotype of E. duckei was also designated to stabilize the application of the name.

Organ-specific volatiles from Sonoran desert Krameria flowers as potential signals for oil-collecting bees

The evolution of flowers that offer oils as rewards and are pollinated by specialized bees represents a distinctive theme in plant-pollinator co-diversification. Some plants that offer acetylated glycerols as floral oils emit diacetin, a volatile by-product of oil metabolism, which is utilized by oil-collecting bees as an index signal for the presence of floral oil. However, floral oils in the genus Krameria (Krameriaceae) contain β-acetoxy-substituted fatty acids instead of acetylated glycerols, making them unlikely to emit diacetin as an oil-bee attractant. We analyzed floral headspace composition from K. bicolor and K. erecta, native to the Sonoran Desert of southwestern North America, in search of alternative candidates for volatile index signals. Using solid-phase microextraction, combined with gas chromatography-mass spectrometry, we identified 26 and 45 floral volatiles, respectively, from whole flowers and dissected flower parts of these two Krameria species. As expected, diacetin was not detected. Instead, β-ionone emerged as a strong candidate for an index signal, as it was uniquely present in dissected oil-producing floral tissues (elaiophores) of K. bicolor, as well as the larval cells and provisions from its oil-bee pollinator, Centris cockerelli. This finding suggests that the floral oil of K. bicolor is perfused with β-ionone in its tissue of origin and retains the distinctive raspberry-like scent of this volatile after being harvested by C. cockerelli bees. In contrast, the elaiophores of K. erecta, which are not thought to be pollinated by C. cockerelli, produced a blend of anise-related oxygenated aromatics not found in the elaiophores of K. bicolor. Our findings suggest that β-ionone has the potential to impact oil-foraging by C. cockerelli bees through several potential mechanisms, including larval imprinting on scented provisions or innate or learned preferences by foraging adults.

Floral resources of Epicharis flava (Hymenoptera, Apidae) in an urban area, detected from the pollen spectrum in the scopae

Bees are the main pollinators of terrestrial ecosystems and, among them, we can highlight oil-collecting bees, which show different morphological and behavioral adaptations associated with plants that offer this floral resource. Floral oils are used in provisioning, building, and lining the brood cell and nests. The genus Epicharis has a neotropical distribution and females are closely associated with plants of the Malpighiaceae family, with the highest number of records in species of the genus Byrsonima. However, due to the strong seasonality of adult activity and solitary behavior, knowledge about important floral resources to Epicharis bees is still scarce. In order to identify important resource sources for a widely distributed species, the current work aimed to analyze the pollen spectrum of Epicharis flava Friese in an urban area in the Atlantic Forest domain. For this, females of E. flava were captured during five days while visiting flowers of Byrsonima sericea DC. (Malpighiaceae) in an urban area, and the pollen load in their scopae was submitted to acetolysis processing for further analysis under the microscope. In total, 71 pollen types were found, with emphasis on Fabaceae, Solanaceae, Bignoniaceae, and Malpighiaceae, considered sources of nectar, pollen, and floral oils. This study made it possible, through the analysis of pollen in the scopae, to identify a list of potentially important species for the maintenance of E. flava populations. This information is necessary for the management of urban green areas, aiming at increasing biodiversity. In addition, these data can serve as a base for further research on oil-collecting bees in the Neotropics.

Floral signals of the dimorphic oil-producing Byrsonima sericea (Malpighiaceae): is the eglandular morph deceptive?

ABSTRACT Background Presence of eglandular individuals (lacking floral oil glands) within populations of several neotropical Malpighiaceae is intriguing, with ecological and evolutionary implications so far unexplored. This floral dimorphism (glandular and eglandular individuals) is hypothesised to be related to energetic costs of oil production and pollinator deception. Aims To evaluate whether eglandular individuals of Byrsonima sericea deceive oil-collecting bees and obtain higher reproductive success (fruit production) compared to glandular individuals. Methods We monitored flower visitation and quantified and identified floral cues (visual and olfactory) associated with glandular and eglandular individuals, and measured fruit set. Results Both morphotypes exhibited similar visual cues and proportions of visits by oil-collecting bees and similar fruit set. Floral scent via headspace analysis indicated no between-morphotype differences in biogenic volatile organic compounds, whilst flower extract samples showed a clear difference in chemical composition. Conclusions Absence of oil production in B. sericea was not associated with changes in floral cues used in pollinator attraction at long distances. Maintenance of floral cues may be a deceptive mechanism that maintains the oil-collecting behaviour of bees on flowers that lack oil glands. Higher fruit set was not observed in eglandular individuals, suggesting that energetic costs associated with oil production do not involve fruit production.

New species of Centris (Xanthemisia) Moure from the Mesoamerican Dominion and the Mexican Transition Zone (Hymenoptera: Apidae).

Three new species of oil-collecting bees of the genus Centris (Xanthemisia) Moure are described and illustrated: C. jakalteka sp. nov., C. maya sp. nov. and C. purhepecha sp. nov. The new proposed taxa are distributed in the north of the Neotropical Region, specifically in the Mesoamerican Dominion and the Mexican Transition Zone, between the Neotropics and Nearctic. In addition, a distribution map and an identification key for the species of the subgenus occurring in the aforementioned regions are also presented.

Pollination failure in Tritoniopsis parviflora (Iridaceae): New insights into the ecology and anatomy of this oil- and nectar-producing species

Pollination in the South African species Tritoniopsis parviflora is of particular interest as it is the only oil-producing member of Iridaceae outside the Americas and the only species in the family known to secrete both floral oil and nectar. We evaluated oil and nectar secretion dynamics of T. parviflora, identified floral visitors and characterized their foraging behavior, and quantified reproductive success. Chemical and anatomical analyses suggest temporal segregation in rewards offered in male and female phases of the protandrous flowers. The diacetin amount was vestigial and none of the bees observed on flowers were specialist oil-collecting bees. Fruit set in the four studied populations was very low (c. 16 % of flowers). These results suggest that the T. parviflora pollination may be ensured by different functional bee groups and the visits by nectar-feeding and pollen-collecting bees may have been supplementary for seed production in the study period in conditions of low abundance of oil bees. The diversity of rewards in T. parviflora may serve as a form of bet-hedging that allows for pollination by generalist bees in the face of unreliable pollination service by specialist oil-collecting bees.

Sensitivity of the Neotropical Solitary Bee Centris analis F. (Hymenoptera, Apidae) to the Reference Insecticide Dimethoate for Pesticide Risk Assessment.

Currently, only Apis mellifera is used in environmental regulation to evaluate the hazard of pesticides to pollinators. The low representativeness of pollinators and bee diversity in this approach may result in insufficient protection for the wild species. This scenario is intensified in tropical environments, where little is known about the effects of pesticides on solitary bees. We aimed to calculate the medium lethal dose (LD50) and medium lethal concentration (LC50) of the insecticide dimethoate in the Neotropical solitary bee Centris analis, a cavity-nesting, oil-collecting bee distributed from Brazil to Mexico. Males and females of C. analis were exposed orally to dimethoate for 48 h under laboratory conditions. Lethality was assessed every 24 h until 144 h after the beginning of the test. After the LD50 calculation, we compared the value with available LD50 values in the literature of other bee species using the species sensitivity distribution curve. In 48 h of exposure, males showed an LD50 value 1.33 times lower than females (32.78 and 43.84 ng active ingredient/bee, respectively). Centris analis was more sensitive to dimethoate than the model species A. mellifera and the solitary bee from temperate zones, Osmia lignaria. However, on a body weight basis, C. analis and A. mellifera had similar LD50 values. Ours is the first study that calculated an LD50 for a Neotropical solitary bee. Besides, the results are of crucial importance for a better understanding of the effects of pesticides on the tropical bee fauna and will help to improve the risk assessment of pesticides to bees under tropical conditions, giving attention to wild species, which are commonly neglected. Environ Toxicol Chem 2023;42:2758-2767. © 2023 SETAC.

Primer registro de la abeja colectora de óleo Centris (Odontoxys) melanochlaena Smith, 1874 (Hymenoptera, Apidae) en Nicaragua

The first report of the oil-collecting bee Centris (Odontoxys) melanochlaena Smith, 1874 in Nicaragua is presented. This species occurs in several Central American countries and Mexico, being this the first record from western Nicaragua. This record contributes to the knowledge of the distribution range of this species, as well as increases the list of native bees occurring in Nicaragua.

Oil flowers and related oil-collecting bees: a 50-year timeline of knowledge and future directions

Oil flowers and related oil-collecting bees: a 50-year timeline of knowledge and future directions

Gut microbiota variation of a tropical oil-collecting bee species far exceeds that of the honeybee.

Interest for bee microbiota has recently been rising, alleviating the gap in knowledge in regard to drivers of solitary bee gut microbiota. However, no study has addressed the microbial acquisition routes of tropical solitary bees. For both social and solitary bees, the gut microbiota has several essential roles such as food processing and immune responses. While social bees such as honeybees maintain a constant gut microbiota by direct transmission from individuals of the same hive, solitary bees do not have direct contact between generations. They thus acquire their gut microbiota from the environment and/or the provision of their brood cell. To establish the role of life history in structuring the gut microbiota of solitary bees, we characterized the gut microbiota of Centris decolorata from a beach population in Mayagüez, Puerto Rico. Females provide the initial brood cell provision for the larvae, while males patrol the nest without any contact with it. We hypothesized that this behavior influences their gut microbiota, and that the origin of larval microbiota is from brood cell provisions. We collected samples from adult females and males of C. decolorata (n = 10 each, n = 20), larvae (n = 4), and brood cell provisions (n = 10). For comparison purposes, we also sampled co-occurring female foragers of social Apis mellifera (n = 6). The samples were dissected, their DNA extracted, and gut microbiota sequenced using 16S rRNA genes. Pollen loads of A. mellifera and C. decolorata were analyzed and interactions between bee species and their plant resources were visualized using a pollination network. While we found the gut of A. mellifera contained the same phylotypes previously reported in the literature, we noted that the variability in the gut microbiota of solitary C. decolorata was significantly higher than that of social A. mellifera. Furthermore, the microbiota of adult C. decolorata mostly consisted of acetic acid bacteria whereas that of A. mellifera mostly had lactic acid bacteria. Among C. decolorata, we found significant differences in alpha and beta diversity between adults and their brood cell provisions (Shannon and Chao1 p < 0.05), due to the higher abundance of families such as Rhizobiaceae and Chitinophagaceae in the brood cells, and of Acetobacteraceae in adults. In addition, the pollination network analysis indicated that A. mellifera had a stronger interaction with Byrsonima sp. and a weaker interaction with Combretaceae while interactions between C. decolorata and its plant resources were constant with the null model. Our data are consistent with the hypothesis that behavioral differences in brood provisioning between solitary and social bees is a factor leading to relatively high variation in the microbiota of the solitary bee.

The primary types of some species of Centris bees described by European entomologists in the 18th and 20th centuries (Hymenoptera: Apidae)

In this paper are presented notes on the primary types of some species of the oil-collecting bees of the genus Centris described by the European naturalists and entomologists Amédée Louis Michel Lepeletier de Saint-Fargeau, Anders Christian Jensen-Haarup, Arthur Louis Marie Joseph Vachal, Charles Émile Blanchard, Embrik Strand, Félix Édouard Guérin-Méneville, Guillaume-Antoine Olivier, Jean Guillaume Audinet-Serville, Jean Pérez, Johann Christoph Friedrich Klug, Johann Ludwig Christ, John Obadiah Westwood, Josef Anton Maximilian Perty, Jules Dominique, Karl Hermann Konrad Burmeister, Karl Wilhelm von Dalla Torre, Massimiliano Spinola, Peter Cameron, and Wilhelm Ferdinand Erichson. Information on the type status, type locality and depository are provided. In order to stabilize some names, lectotype designations were made for Centris rhodophthalma, C. sponsa var. asuncionis, C. transversa, Hemisia byssina and Ptilotopus americanus. Centris sponsa var. asuncionis is withdrawn from the synonymy of C. sponsa, revalidated and raised to species level. Centris byssina is proposed as nomen oblitum and as a new junior synonym of C. trigonoides, nomen protectum.

Notas taxonômicas sobre os tipos primários de algumas espécies de abelhas do gênero Centris descritas por alguns entomologistas das Américas (Hymenoptera: Apidae)

ABSTRACT In this paper are presented notes on the primary types of some species of the oil-collecting bees of the genus Centris Fabricius, 1804 described by Alpheus Packard, Arturo Roig-Alsina, Charles Michener, Flamínio Ruiz, Haroldo Toro, James Crawford, Jesus Santiago Moure, Philip Timberlake, and Roy Snelling. Information on the type status, type locality and depository are provided.

Are the floral morphology and anatomy of Galphimia australis, an atypical neotropical Malpighiaceae, associated to a new pollination syndrome?

The flowers of the species of Malpighiaceae in the Neotropical Region are relatively uniform in their morphology due to their dependence on oil-collecting bees as their main pollinators. However, many species of the genus Galphimia seem to have acquired a different floral syndrome, lacking markedly zygomorphic flowers and developed elaiophores in the calyx. Likewise, these species present anthers with great development, probably in response to the selection of pollinators that collect pollen. Galphimia australis incorporated some of these traits but also retained some residual characteristics typical of species pollinated by oil bees. This leads to many questions on how these flowers ensure their pollination. Inquiring about the reduction or modification of these characteristics allows us to understand how G. australis achieves a different pollination syndrome. In this research, we carry out a detailed morphological and anatomical study of the flowers and pollen grain devolvement of G. australis and floral visitors were observed and captured. Results were analyzed in order to determine how this species changed from the oil-floral syndrome, typical of neotropical Malpighiaceae, to one syndrome with pollen as the main reward.

Variación interespecífica de ensambles de polinizadores en Nierembergia (Solanaceae) en relación con la localización geográfica y la variación fenotípica de las flores

Understanding how the interactions of related plant species with pollinators vary on a spatial scale provides the opportunity to establish links between macroevolutionary patterns and microevolutionary processes, as well as to approach the mechanisms underlying plant diversification. In this work, we explore the variation in pollinator assemblages of 15 species and varieties of Nierembergia (Solanaceae) across the distribution range of the genus in Argentina, in relation to variation in floral phenotype and geographic location. By field observations, morphometric measurements of flowers and comparative phylogenetic methods, pollinator assemblages and flowers of Nierembergia taxa were characterized and compared, and the association between pollinator assemblage composition, geographic location, floral morphology and phylogenetic relationships was evaluated. 13 species of oil-collecting bees were recorded as pollinators. The assemblage composition was strongly associated with geographic location, that is, Nierembergia taxa in nearby areas had greater similarity in their pollinator assemblages than geographically distant taxa. This pattern was not associated with phylogenetic relationships among taxa, except for a group of high mountain species in northwestern Argentina. On the other hand, interspecific variation was found in the floral phenotype, mainly in the corolla and the oil-producing gland size. However, Nierembergia taxa with similar floral phenotypes did not share the composition of the pollinator assemblage, as expected. In conclusion, we found a mixed macroevolutionary pattern in which some phylogenetically distant Nierembergia taxa converge geographically in the composition of pollinator assemblages, while this attribute is conserved in a phylogenetic clade. This pattern suggests that the role of pollinators in Nierembergia diversification is more complex than previously thought.

Oil flowers of Malpighiaceae and its oil-collecting bees: loyalty and robbery in a highly specialized system

Oil flowers of Malpighiaceae and its oil-collecting bees: loyalty and robbery in a highly specialized system