Bee Tribe Research Articles

Antiquity of cleptoparasitism among bees revealed by morphometric and phylogenetic analysis of a Paleocene fossil nomadine (Hymenoptera: Apidae)

AbstractCleptoparasitism is a way of life involving the theft of resources by one animal from another. This behaviour occurs in many bee tribes but its origin and evolution remain obscure, particularly owing to the relative scarcity of bees in the fossil record. Hitherto, no fossil evidence has been recorded to trace the origin of cleptoparasitim among bees. In the current study, we present the first cleptoparasitic bee fossil, providing analyses of its taxonomic affinities and a complete description. The specimen also happens to be one of the earliest bee fossils, having been discovered in the spongo‐diatomitic volcanic paleolake of Menat (Paleocene) in France. We employed geometric morphometrics of the forewing shape to assess the taxonomic affinities of the fossil with modern apoid tribes. Our dataset included 979 specimens representing 50 tribes and 225 extant species. Based on linear and geometric morphometrics, we demonstrate that the fossil's forewing shape is similar to that of Apidae, and particularly to that of the tribe Epeolini (Nomadinae). The fossil is described as Paleoepeolus micheneri gen.n., sp.n. and provides the first direct evidence on the antiquity of cleptoparasitism among bees.This published work has been registered in ZooBank, http://zoobank.org/urn:lsid:zoobank.org:pub:BBBE22176CAE48F9851F716B813DFEBF.

Discovery of the Bee Tribe Tarsaliini in Arabia (Hymenoptera: Apidae), with the Description of a New Species

ABSTRACT The uncommonly encountered bee tribe Tarsaliini (Apinae) is recorded from the Arabian Peninsula for the first time, and based on a new species of the genus Tarsalia Morawitz. The tribes Ancylaini and Tarsaliini are diagnosed and their differences highlighted. Tarsalia kindahensis Engel, new species, is described and figured from the eastern portion of the Najd of central-eastern Saudi Arabia (Qassim and Riyadh regions). The new species is most similar to T. mimetes (Cockerell), known only from Egypt and Sudan, as well as the larger T. persica (Warncke) from Iran. These three species are morphologically and largely geographically distinct from the remainder of the genus, and are segregated into a new subgenus, Astibomelissa Engel. An updated and corrected checklist of the genera and subgenera of bees recorded from Saudi Arabia is appended.

Taxonomy and ecology of a new species of Corynura (Hymenoptera:Halictidae: Augochlorini) from Chile and Argentina.

We describe a new species of Corynura Spinola, a socially polymorphic genus within the bee tribe Augochlorini (Halictidae). We present a detailed description of both sexes of Corynura (Corynura) moscosensis n. sp. González-Vaquero, images of diagnostic morphological structures and antennal sensilla, floral associations, distributional data and notes on its nesting biology. Corynura moscosensis n. sp. is similar in appearance to C. (C.) chloromelas (Alfken), but it can be distinguished by the sculpturing of the mesoscutum and the hair types on the propodeum in the female, and by the genitalia and extent of the area exclusively covered by sensilla placoidea on the antennal flagellum of the male. A lectotype is designated for C. chloromelas. A Chilean Patagonian population of C. moscosensis n. sp. was observed to dig spatially clumped nests in an earth bank with a moderately hard and humid soil. The presence of multiple females within single nest tunnels is unusual and may preliminary suggest nest-sharing, but more data are necessary to define the social organization of this species. The species appears to be polylectic. Bee nests were attacked by satellite flies and possibly velvet ants.

Absence of Leishmaniinae and Nosematidae in stingless bees.

Bee pollination is an indispensable component of global food production and plays a crucial role in sustainable agriculture. The worldwide decline of bee populations, including wild pollinators, poses a threat to this system. However, most studies to date are situated in temperate regions where Apini and Bombini are very abundant pollinators. Tropical and subtropical regions where stingless bees (Apidae: Meliponini) are generally very common, are often overlooked. These bees also face pressure due to deforestation and agricultural intensification as well as the growing use and spread of exotic pollinators as Apis mellifera and Bombus species. The loss or decline of this important bee tribe would have a large impact on their provided ecosystem services, in both wild and agricultural landscapes. The importance of pollinator diseases, which can contribute to decline, has not been investigated so far in this bee tribe. Here we report on the first large pathogen screening of Meliponini species in southern Brazil. Remarkably we observed that there was an absence of Leishmaniinae and Nosematidae, and a very low occurrence of Apicystis bombi. Our data on disease prevalence in both understudied areas and species, can greatly improve our knowledge on the distribution of pathogens among bee species.

Temporal niche overlap and distinct bee ability to collect floral resources on three species of Brazilian Malpighiaceae

Spatial and temporal limited resource and niche overlap studies have been widely used to explain resource-sharing in community ecology. Furthermore, morphological and behavioral differences among species are relevant to predict how they may share niche availabilities. We evaluated temporal niche overlap and the ability of visitors to collect floral resources on three Malpighiaceae species in the Brazilian savannah. We hypothesized: (I) an overlap between the temporal niches due the similarities between their floral resources requirements and the temporal limitation of flowering; and (II) a differential ability of bee species in resource harvesting. The 31 floral visitor species exhibited a higher niche overlap than expected by chance, confirming our first hypothesis. Furthermore, according to our second hypothesis, we observed that floral visitors showed a different efficiency in resource collection, depending on bee size and behavior. We believe that this may be a proxy of pollination efficiency. Our discussion is based on the distinct specialization of oil-collecting abilities and the specific requirements of each bee tribe.

Comprehensive phylogeny, biogeography and new classification of the diverse bee tribe Megachilini: Can we use DNA barcodes in phylogenies of large genera?

Classification and evolutionary studies of particularly speciose clades pose important challenges, as phylogenetic analyses typically sample a small proportion of the existing diversity. We examine here one of the largest bee genera, the genus Megachile – the dauber and leafcutting bees. Besides presenting a phylogeny based on five nuclear genes (5480 aligned nucleotide positions), we attempt to use the phylogenetic signal of mitochondrial DNA barcodes, which are rapidly accumulating and already include a substantial proportion of the known species diversity in the genus. We used barcodes in two ways: first, to identify particularly divergent lineages and thus to guide taxon sampling in our nuclear phylogeny; second, to augment taxon sampling by combining nuclear markers (as backbone for ancient divergences) with DNA barcodes. Our results indicate that DNA barcodes bear phylogenetic signal limited to very recent divergences (3–4 my before present). Sampling within clades of very closely related species may be augmented using this technique, but our results also suggest statistically supported, but incongruent placements of some taxa. However, the addition of one single nuclear gene (LW-rhodopsin) to the DNA barcode data was enough to recover meaningful placement with high clade support values for nodes up to 15 million years old. We discuss different proposals for the generic classification of the tribe Megachilini. Finding a classification that is both in agreement with our phylogenetic hypotheses and practical in terms of diagnosability is particularly challenging as our analyses recover several well-supported clades that include morphologically heterogeneous lineages. We favour a classification that recognizes seven morphologically well-delimited genera in Megachilini: Coelioxys, Gronoceras, Heriadopsis, Matangapis, Megachile, Noteriades and Radoszkowskiana. Our results also lead to the following classification changes: the groups known as Dinavis, Neglectella, Eurymella and Phaenosarus are reestablished as valid subgenera of the genus Megachile, while the subgenus Alocanthedon is placed in synonymy with M. (Callomegachile), the subgenera Parachalicodoma and Largella with M. (Pseudomegachile), Anodonteutricharaea with M. (Paracella), Platysta with M. (Eurymella), and Grosapis and Eumegachile with M. (Megachile) (new synonymies). In addition, we use maximum likelihood reconstructions of ancestral geographic ranges to infer the origin of the tribe and reconstruct the main dispersal routes explaining the current, cosmopolitan distribution of this genus.

Phylogenetic systematics and a revised generic classification of anthidiine bees (Hymenoptera: Megachilidae)

The bee tribe Anthidiini (Hymenoptera: Megachilidae) is a large, cosmopolitan group of solitary bees that exhibit intriguing nesting behavior. We present the first molecular-based phylogenetic analysis of relationships within Anthidiini using model-based methods and a large, multi-locus dataset (five nuclear genes, 5081 base pairs), as well as a combined analysis using our molecular dataset in conjunction with a previously published morphological matrix. We discuss the evolution of nesting behavior in Anthidiini and the relationship between nesting material and female mandibular morphology. Following an examination of the morphological characters historically used to recognize anthidiine genera, we recommend the use of a molecular-based phylogenetic backbone to define taxonomic groups prior to the assignment of diagnostic morphological characters for these groups. Finally, our results reveal the paraphyly of numerous genera and have significant consequences for anthidiine classification. In order to promote a classification system based on stable, monophyletic clades, we hereby make the following changes to Michener’s (2007) classification: The subgenera Afranthidium (Zosteranthidium) Michener and Griswold, 1994, Afranthidium (Branthidium) Pasteels, 1969 and Afranthidium (Immanthidium) Pasteels, 1969 are moved into the genus Pseudoanthidium, thus forming the new combinations Pseudoanthidium (Zosteranthidium), Pseudoanthidium (Branthidium), and Pseudoanthidium (Immanthidium). The genus Neanthidium Pasteels, 1969 is also moved into the genus Pseudoanthidium, thus forming the new combination Pseudoanthidium (Neanthidium).Based on morphological characters shared with our new definition of the genus Pseudoanthidium, the subgenus Afranthidium (Mesanthidiellum) Pasteels, 1969 and the genus Gnathanthidium Pasteels, 1969 are also moved into the genus Pseudoanthidium, thus forming the new combinations Pseudoanthidium (Mesanthidiellum) and Pseudoanthidium (Gnathanthidium).

A molecular and morphological phylogeny of the extant Augochlorini (Hymenoptera, Apoidea) with comments on implications for biogeography

AbstractThe Augochlorini Beebe is a New World tribe of bees comprising 663 described species. Relationships among the genera of this monophyletic tribe remain uncertain. Here I provide a comprehensive phylogeny using morphological and molecular information. In all, 54 Augochlorini species plus 16 outgroups and 3017 molecular and 105 morphological characters were analysed. Sequences for four genes were analysed using Bayesian inference, maximum likelihood and parsimony. Morphological characters were taken from a literature review and analysed alone and in combination with molecular data using parsimony. The monophyly of Augochlorini and most genera is confirmed, with divergence of the main lineages of the tribe around 55–20 Ma. Seven clades were supported by most analyses and are here treated as genus‐level groups, as follows (combined analysis topology): (Corynura group, (Chlerogella group, (Rhinocorynura group, (Augochloropsis, (Megaloptidia group, (Neocorynura group, (Augochlora group, Megalopta group))))))). According to this topology, dim‐light foraging and cleptoparasitism arose three times in the tribe. According to my hypothesis, the diversification of Augochlorini may have begun as a response to vicariant events, including the split of the Neotropical/Andean regions and marine transgressions in the Amazon region.

The Problems of a Priori Categorisation of Agonism and Cooperation: Circle‐Tube Interactions in Two Allodapine Bees

AbstractCircle‐tube experiments have been widely used to both examine nestmate recognition in social and solitary insects, as well as to characterise interactions in terms of agonism, cooperation, and avoidance. Despite their use in studies of halictid bees, carpenter bees, adrenid bees, and wasps, they have never been used to explore social interactions in the bee tribe Allodapini, where sociality varies widely in terms of complexity. Here, we investigate behaviours displayed within the highly eusocial allodapine Exoneurella tridentata and the facultatively social Exoneura robusta, using a standardised circle‐tube apparatus. We present two broad and important results: (i) Discrimination between nestmates and non‐nestmates is much more strongly expressed in the facultatively social species and (ii) principal components analyses do not indicate suites of behaviours that permit clear interpretations as being agonistic, cooperative, or avoidance. Our first set of results suggests that nestmate recognition is not an essential ability for social species. Our second set of results raise important questions about a priori functional categorisations of behaviours and whether these can be used to reliably classify observed behaviours as either avoidance, cooperation, or aggression. Our analyses highlight the risks of interpreting social insect interactions and call for a more cautious approach.

Heterochrony of cuticular differentiation in eusocial corbiculate bees

AbstractThe exoskeleton (cuticle) of insects varies widely in shape, biomechanical properties, and functions, which are inherent to the biological species and developmental stage, besides showing a wealth of architectural specializations and nuances in the different body regions. The morphological pattern of exoskeleton maturation was studied in eusocial and solitary bees, including species of all three eusocial tribes of corbiculate bees as follows: Apini, Meliponini, and Bombini. The results showed striking differences in the rate of cuticle maturation between the solitary bees that leave the nest soon after the adult ecdysis, and the eusocial bees that take longer to leave the colony for foraging activities. There was a clear delay in the post-ecdysial cuticle tanning (melanization and sclerotization) in the eusocial bee species in comparison to the solitary species, suggesting adaptation to sociality and to the protective environment of the colony. Such heterochrony of cuticle maturation seems a conserved ontogenetic trait related to the way of life in corbiculate bees. The data generated a basic framework of exoskeleton maturation in corbiculate bees, under ontogenetic and evolutionary approaches, and give experimental support for further research on adaptation to the colony environment.

Sexual dimorphism in the olfactory system of a solitary and a eusocial bee species

Sexually dimorphic sensory systems are common in Hymenoptera and are considered to result from sex-specific selection pressures. An extreme example of sensory dimorphism is found in the solitary bee tribe Eucerini. Males of long-horned bees bear antennae that exceed body length. This study investigated the pronounced sexual dimorphism of the peripheral olfactory system and its representation in higher brain centers of the species Eucera berlandi. Eucera males have elongated antennae, with 10 times more pore plates and three times more olfactory receptor neurons than females. The male antennal lobe (AL) comprises fewer glomeruli than the female AL (∼100 vs. ∼130), of which four are male-specific macroglomeruli. No sex differences were found in the relative volume of the mushroom bodies, a higher order neuropil essential for learning and memory in Hymenoptera. Compared with the Western honeybee, the degree of sexual dimorphism in Eucera is more pronounced at the periphery. In contrast, sex differences in glomerular numbers are higher in the eusocial honeybee and a sexual dimorphism of the relative investment in mushroom body tissue is observed only in Apis. The observed differences between the eusocial and the solitary bee species may reflect differences in male-specific behavioral traits and associated selection pressures, which are discussed in brief.

Repeated origins of social parasitism in allodapine bees indicate that the weak form of Emery's rule is widespread, yet sympatric speciation remains highly problematic

The evolutionary origins of social parasitism are very unevenly distributed among ants, bees and wasps, but social parasite lineages are frequently close relatives of their host lineages. Two explanations for these relationships have been proposed: (1) initially, social species are more likely to become parasitic on relatively closely related social species, because they share life history, physiological and behavioural traits that allow successful integration within the host colony; and (2) social parasites have evolved directly from their host lineage via sympatric speciation. Comparative approaches, covering multiple origins and intermediate evolutionary stages, are needed to determine which of these possibilities is more likely. We use molecular phylogenetics to examine multiple origins of parasitism in the bee tribe Allodapini. We identify seven origins resulting in obligate social parasitism (inquilinism), one origin of facultative social parasitism, which was followed by subsequent speciation and where both daughter species remained facultatively parasitic, and one case of frequent facultative heterospecific co-nesting that probably represents incipient social parasitism. All host–parasite lineage pairs show strong phylogenetic affinities, but only the case of facultative heterospecific nesting involves true sister species relationships. Our results are consistent with the range of parasitic relationships that are expected under an allopatric model for the origin of social parasitism, but are highly problematic for a sympatric speciation model. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109, 320–331.

Diversity and evolutionary patterns of bacterial gut associates of corbiculate bees

The animal gut is a habitat for diverse communities of microorganisms (microbiota). Honeybees and bumblebees have recently been shown to harbour a distinct and species poor microbiota, which may confer protection against parasites. Here, we investigate diversity, host specificity and transmission mode of two of the most common, yet poorly known, gut bacteria of honeybees and bumblebees: Snodgrassella alvi (Betaproteobacteria) and Gilliamella apicola (Gammaproteobacteria). We analysed 16S rRNA gene sequences of these bacteria from diverse bee host species across most of the honeybee and bumblebee phylogenetic diversity from North America, Europe and Asia. These focal bacteria were present in 92% of bumblebee species and all honeybee species but were found to be absent in the two related corbiculate bee tribes, the stingless bees (Meliponini) and orchid bees (Euglossini). Both Snodgrassella alvi and Gilliamella apicola phylogenies show significant topological congruence with the phylogeny of their bee hosts, albeit with a considerable degree of putative host switches. Furthermore, we found that phylogenetic distances between Gilliamella apicola samples correlated with the geographical distance between sampling locations. This tentatively suggests that the environmental transmission rate, as set by geographical distance, affects the distribution of G.apicola infections. We show experimentally that both bacterial taxa can be vertically transmitted from the mother colony to daughter queens, and social contact with nest mates after emergence from the pupa greatly facilitates this transmission. Therefore, sociality may play an important role in vertical transmission and opens up the potential for co-evolution or at least a close association of gut bacteria with their hosts.

A new species of Centris (Paracentris) Cameron, 1903 from northeastern Brazil, with a key for the Centris species of the Caatinga region (Hymenoptera: Apidae)

Centris (Paracentris) Cameron is one of the subgenera with the greatest species richness of the bee tribe Centridini. Inthis paper, Centris nordestina, a new Brazilian species of the subgenus is described, and due to its close relationship witha clade of Andean species, a new biogeographical track is defined uniting northeastern Brazil with the Andes. For the first time a key for the species of the Caatinga region, the semiarid region of northeastern Brazil, is provided.

Descriptions of Mature Larvae of the Bee Tribe Emphorini and Its Subtribes (Hymenoptera, Apidae, Apinae)

A description of the mature larvae of the bee tribe Emphorini based on representatives of six genera is presented herein. The two included subtribes, Ancyloscelidina and Emphorina, are also characterized and distinguished from one another primarily by their mandibular anatomy. The anatomy of abdominal segments 9 and 10 is investigated and appears to have distinctive features that distinguish the larvae of the tribe from those of related apine tribes.

The evolution of eusociality in allodapine bees: workers began by waiting

Understanding how sterile worker castes in social insects first evolved is one of the supreme puzzles in social evolution. Here, we show that in the bee tribe Allodapini, the earliest societies did not entail a foraging worker caste, but instead comprised females sharing a nest with supersedure of dominance. Subordinates delayed foraging until they became reproductively active, whereupon they provided food for their own brood as well as for those of previously dominant females. The earliest allodapine societies are, therefore, not consistent with an 'evo-devo' paradigm, where decoupling of foraging and reproductive tasks is proposed as a key early step in social evolution. Important features of these ancestral societies were insurance benefits for dominants, headstart benefits for subordinates and direct reproduction for both. The two lineages where morphologically distinct foraging worker castes evolved both occur in ecosystems with severe constraints on independent nesting and where brood rearing periods are very seasonally restricted. These conditions would have strongly curtailed dispersal options and increased the likelihood that dominance supersedure occurred after brood rearing opportunities were largely degraded. The origins of foraging castes, therefore, represented a shift towards assured fitness gains by subordinates, mediated by the dual constraints of social hierarchies and environmental harshness.

Phylogenetic Analysis of the Bee Tribe Anthidiini

The phylogenetic relationships among members of long tongue bee tribe Anthidiini (Megachilidae: Megachilinae) were investigated at the Department of Entomology and Wildlife, University of Cape Coast (Ghana) and the Agricultural Research Council, Pretoria (South Af-rica) from July, 2006 to May, 2007. Ten museums located in three continents loaned the 990 specimens used for the studies. Thirty-three ingroup taxa out of the 37 known genera of the world’s Anthidiini and two outgroup genera, were included in a cladistic analysis of the tribe based on 51 adult external morphological characters. The cladograms yielded three major clades which have been erected as subtribes for the world’s Anthidiini, namely Afranthidina, Anthidina and Euaspina. Monophyly of the Anthidiini was confirmed. Based on the result of the cladistic analysis and biogeographic data, it is suggested that the origin and center of radiation for the Anthidiini probably occurred in the southern pantropic region (Southern Africa to South East Asia) of Gondwana. A second and independent migration to the Neotropical region by the prob-able ancestors of the current Neotropic genera is also conceivable.

Social polymorphism in the Australian small carpenter bee, Ceratina (Neoceratina) australensis

The bee tribe Ceratinini provides important insights into the early stages of sociality. Many arthropods exhibit behaviours precursory to social life, including adult longevity, parental care, nest loyalty and mutual tolerance, yet the origins of social behaviour are few. Here we describe the biology of a facultatively social bee, Ceratina (Neoceratina) australensis, which exhibits all of the preadaptations for successful group living, yet presents ecological and behavioural characteristics that seemingly disfavour frequent colony formation. This species is socially polymorphic with both solitary and social nests collected in sympatry. Social colonies consist of two foundresses, one contributing both foraging and reproductive effort and the second which remains at the nest as a passive guard. Cooperative nesting provides no overt reproductive benefits over solitary nesting in this population, although brood survival tends to be greater in social colonies. Maternal longevity, subsociality and bivoltine nesting phenology in this species favour colony formation, while dispersal habits and offspring longevity may inhibit more frequent social nesting in this and other ceratinines.

New species and unexpected diversity of socially parasitic bees in the genus Inquilina Michener (Hymenoptera: Apoidea: Apidae)

Abstract Allodapine bees present particular problems for taxonomy due to a high level of morphological conservatism in adults, even between genera. However, this tribe of bees also presents a unique opportunity to explore the evolution of social parasitism because of the comparatively large number of origins of socially parasitic species. Morphological differences presented here, along with DNA sequence data and molecular phylogenetic analyses, indicate a much larger number of Australian social parasite species in the genus Inquilina than previously anticipated, and suggest that the final number of socially parasitic species may be considerable. We describe five new species and present sequence data that will help elucidate the delineation of further new species. Inquilina provides a unique opportunity to study the evolution of social parasitism in social insects, but further studies will need to encompass both population genetic and phylogenetic approaches.

Evidence of Social Nesting in the Ceratina of Borneo (Hymenoptera: Apidae)

The bee tribe Ceratinini is important for understanding early stages in social evolution. Their extant sister tribe Allodapini contains no strictly solitary species, and while some Ceratinini are commonly regarded as solitary, little behavioural data exist to substantiate this. Studies on Asian congeners have shown recurrent sociality in temperate and subtropical ranges while behavioural data are lacking in tropical regions. Field work along the west coast of Borneo in Sarawak, Malaysia, has provided some insight into these tropical taxa. Here we describe the nesting biology and social behaviour of four taxonomically described yet behaviourally unclassified Ceratina species. These four species are from three subgenera, namely Ceratina (Ceratinidia) accusator Cockerell, C. (Ceratinidia) nigrolateralis Cockerell, C. (Neoceratina) dentipes Friese, C. (Pithitis) smaragdula Fabricius. Nests of all species were typically attended by an adult female while all species except C. accusator had a low frequency of multi-female nesting assemblages. The four tropical ceratinines described here and all other behaviourally classified species exhibit recurrent patterns of maternal care, maternal longevity, and nest protection. Prolonged parental care found across the genus and occasional transitions into sociality make Ceratina of future interest for the study of life history and social evolution. The evolution of eusociality is considered one of the major transitions in evolution (Maynard Smith and Szathamary, 1995). In solitary species, offspring disperse and reproduce independently whereas workers in eusocial societies remain at the natal nest and largely forego reproduction to aid the queen in rearing siblings. Socially polymorphic lineages, those containing both solitary and social species, retain the plasticity to allow intra-specific comparisons of solitary with social life. The key to understanding the transition to sociality requires a group of closely related taxa possessing broad social, taxonomic and geographic diversity. Bees provide numerous contrasts to offer insights into the origin of sociality with their range of solitary to social forms. The small carpenter bees Hymenoptera: Apidae (Xylocopinae: Ceratinini) are commonly regarded as solitary (Michener, 1974). All behaviourally classified species share a relatively simple life history. Females disperse from their natal nests and find appropriate nesting substrate. These twig-nesting bees excavate linear burrows in the cores of dead exposed pithy stems. Subsequent to burrow construction, females forage for pollen and nectar provisions that they form into a pollen mass on which they lay an egg. After provisioning and oviposition, brood cells are cappe dw ith a partition of wood pith, and the process is repeated in a serial manner along the linear nest chamber.