Eucerini Research Articles

Correction to: UCE phylogenomics, biogeography, and classification of long-horned bees (Hymenoptera: Apidae: Eucerini), with insights on using specimens with extremely degraded DNA

Correction to: UCE phylogenomics, biogeography, and classification of long-horned bees (Hymenoptera: Apidae: Eucerini), with insights on using specimens with extremely degraded DNA

A Distinct Arabidopsis Latent Virus 1 Isolate Was Found in Wild Brassica hirta Plants and Bees, Suggesting the Potential Involvement of Pollinators in Virus Spread.

During our search for aphid-pathogenic viruses, a comovirus was isolated from wild asymptomatic Brassica hirta (white mustard) plants harboring a dense population of Brevicoryne brassicae aphids. The transmission-electron-microscopy visualization of purified virions revealed icosahedral particles. The virus was mechanically transmitted to plants belonging to Brassicaceae, Solanaceae, Amaranthaceae, and Fabaceae families, showing unique ringspot symptoms only on B. rapa var. perviridis plants. The complete viral genome, comprised of two RNA segments, was sequenced. RNA1 and RNA2 contained 5921 and 3457 nucleotides, respectively, excluding the 3' terminal poly-adenylated tails. RNA1 and RNA2 each had one open-reading frame encoding a polyprotein of 1850 and 1050 amino acids, respectively. The deduced amino acids at the Pro-Pol region, delineated between a conserved CG motif of 3C-like proteinase and a GDD motif of RNA-dependent RNA polymerase, shared a 96.5% and 90% identity with the newly identified Apis mellifera-associated comovirus and Arabidopsis latent virus 1 (ArLV1), respectively. Because ArLV1 was identified early in 2018, the B. hirta comovirus was designated as ArLV1-IL-Bh. A high-throughput-sequencing-analyses of the extracted RNA from managed honeybees and three abundant wild bee genera, mining bees, long-horned bees, and masked bees, sampled while co-foraging in a Mediterranean ecosystem, allowed the assembly of ArLV1-IL-Bh, suggesting pollinators' involvement in comovirus spread in weeds.

UCE phylogenomics, biogeography, and classification of long-horned bees (Hymenoptera: Apidae: Eucerini), with insights on using specimens with extremely degraded DNA

AbstractLong-horned bees (Apidae, Eucerini) are found in different biomes worldwide and include some important crop pollinators. In the Western Hemisphere, Eucerini received extensive taxonomic study during the twentieth century, resulting in several revisions of its genera. In contrast, progress on eucerine phylogenetic research and the genus-level classification has been slow, primarily due to the relatively homogeneous external morphology within the tribe and the rarity of many of its species in collections. Here, we present a comprehensive phylogenetic study of Eucerini based on ultraconserved elements, including 153 species from nearly all genera and subgenera and from all biogeographic regions where they occur. Many of these specimens are from museums and were collected as far back as 1909. We discuss the challenges of working with specimens with highly degraded DNA, present insights into improving phylogenetic results for both species-tree and concatenation approaches, and present a new pipeline for UCE curation (Curation of UltraconseRved Elements—CURE). Our results show the existence of seven main lineages in Eucerini and most of the genera and subgenera to be reciprocally monophyletic. Using a comprehensive and up-to-date phylogenetic framework, we: (1) propose taxonomic changes, including a new subtribal classification and reorganized generic and subgeneric limits; (2) estimate divergence times; and (3) conduct a detailed exploration of historical biogeography of long-horned bees. We find that eucerine lineages expanded their range onto most continents only after their initial diversification in southern South America during the Eocene.

Habitat preference influences response to changing agricultural landscapes in two long-horned bees

Agricultural intensification and urban development have drastically influenced pollinators living in semi-natural grasslands. Pollinators are likely to have different responses to more intensive land uses; some decline rapidly, whereas others maintain or increase their populations. We predicted that differences in interspecific responses to different land uses are partly attributed to differences in habitat preference. We examined the distribution and flower use patterns of two closely related Eucera species with different habitat preferences. Study sites were narrow belt-like meadows within traditional, intensified, and urbanised agricultural lands in the Osaka-Kobe metropolitan area, Japan. Forest-associated Eucera nipponensis were significantly fewer in consolidated and urbanised meadows than in traditional meadows, whereas open land-associated E. spurcatipes exhibited the opposite pattern. A significant negative relationship between their abundance was also found. Both species foraged on legume flowers most frequently (83.5%), but their floral use patterns differed significantly in traditional and consolidated meadows. The bee species that preferred stable habitats were vulnerable to land consolidation and urbanisation, while the species associated with disturbed habitats maintained or increased its population size in meadows with these intensive land uses. Thus, recent land-use changes may have different impacts on species with different habitat preferences.

UCE phylogenomics, biogeography, and classification of long-horned bees (Hymenoptera: Apidae: Eucerini), with insights on using specimens with extremely degraded DNA

UCE phylogenomics, biogeography, and classification of long-horned bees (Hymenoptera: Apidae: Eucerini), with insights on using specimens with extremely degraded DNA

UCE phylogenomics, biogeography, and classification of long-horned bees (Hymenoptera: Apidae: Eucerini), with insights on using specimens with extremely degraded DNA

UCE phylogenomics, biogeography, and classification of long-horned bees (Hymenoptera: Apidae: Eucerini), with insights on using specimens with extremely degraded DNA

New genus and subgenus of South American long-horned bees (Apidae, Eucerini)

As part of a broader treatment of Eucerini systematics, a new genus and a new subgenus are described to accommodate previously described species. Savannychapis gen. n. is described to accommodate Gaesischia interrupta Urban 1989, originally described as a species of Gaesischia (Gaesischiana) Michener et al. 1955, and Gaesischia (Gaesischioides) subgen. n. to accommodate Gaesischia hyptidis (Ducke 1910), previously included in Gaesischia s. str. Michener et al. 1955 and G. (Agaesischia) Moure & Michener 1955. These new taxa are only known in the South American dry diagonal, a set of open vegetation biomes of central-eastern South America.

Bee flowers drive macroevolutionary diversification in long-horned bees.

The role of plant–pollinator interactions in the rapid radiation of the angiosperms have long fascinated evolutionary biologists. Studies have brought evidence for pollinator-driven diversification of various plant lineages, particularly plants with specialized flowers and concealed rewards. By contrast, little is known about how this crucial interaction has shaped macroevolutionary patterns of floral visitors. In particular, there is currently no empirical evidence that floral host association has increased diversification in bees, the most prominent group of floral visitors that essentially rely on angiosperm pollen. In this study, we examine how floral host preference influenced diversification in eucerine bees (Apidae, Eucerini), which exhibit large variations in their floral associations. We combine quantitative pollen analyses with a recently proposed phylogenetic hypothesis, and use a state speciation and extinction probabilistic approach. Using this framework, we provide the first evidence that multiple evolutionary transitions from host plants with accessible pollen to restricted pollen from ‘bee-flowers’ have significantly increased the diversification of a bee clade. We suggest that exploiting host plants with restricted pollen has allowed the exploitation of a new ecological niche for eucerine bees and contributed both to their colonization of vast regions of the world and their rapid diversification.

Landscape Effects on Native Bees (Hymenoptera: Anthophila) Captured in Pheromone Traps for Noctuid Crop Pests (Lepidoptera: Noctuidae).

Noctuid pests, including tobacco budworm (Chloridea virescens (Fab.)) and bollworm (Helicoverpa zea (Boddie)), are significant pests of southern row crops including cotton (Gossypium hirsutum L.), corn (Zea mays L.), and soybean (Glycine max (L.) Moench.). This pest complex is seasonally monitored through Hartstack traps that are baited with synthetic lepidopteran pheromones across the southern United States. We examined bycatch from the noctuid traps deployed across the Mississippi Delta in 2015, 2016, and 2017 for the presence of bees. The most abundant species collected were honey bees (Apis mellifera L.), bumble bees (Bombus spp.), and long-horned bees (Melissodes spp.); these three genera accounted for 82.4% of specimens collected. We also evaluated the proportion of local- and landscape-level habitats on the abundance and richness of the bees caught as bycatch. The proportion of natural and semi-natural habitat affected the abundance and richness of bees collected at the landscape level, but not at more local scales. Additional research is needed to better understand these interactions between bycatch and landscape factors to minimize non-target collections.

How do rewardless Bletilla striata flowers attract pollinators to achieve pollination?

Rewardless plants use various strategies to attract pollinators. Generalized food-deceptive species exploit the nonspecific food-seeking responses of their pollinators. Because past experiences are important for establishing the food-seeking behaviors of insects, previous flower visits by pollinators should play crucial roles in rewardless plants. In this study, we investigated previous experiences of insects that visited the rewardless orchid Bletilla striata based on pollen attached to their bodies to clarify whether experience of visiting flowers with similar colors as rewardless flowers is necessary. Contrary to the expectation, less than half of the flower visitors carried pollen of flowers with similar colors as B. striata, implying that past experience is not essential. Furthermore, we investigated the effects of learning based on the association between the flower position and fruit set assuming that the fruit set would decrease with the progression of the flowering season. A significant association was found at only one of the three study sites. Among flower visitors, male long-horned bees (Eucera spurcatipes) and honeybees (Apis mellifera) primarily carried B. striata pollinia. We hypothesize that B. striata uses generalized food deception to attract honeybees and rendezvous attraction to attract mate-searching male long-horned bees and that this mixed strategy invalidates the associations assumed in generalized food deception.

Bees Occurring in Corn Production Fields Treated with Atoxigenic Aspergillus flavus (Texas, USA)

A saprophytic soil fungus, Aspergillus flavus, produces aflatoxin (toxigenic strains) in the kernels of corn (Zea mays L.) and seeds of many other crops. Many strains of A. flavus do not produce toxigenic aflatoxin, and soil application of these atoxigenic strains is a suppressive control tactic to assist in controlling toxigenic conspecifics. Effects of atoxigenic A. flavus applications on honey bees (Apis mellifera L.) and other bees are unknown, and basic information on bee occurrences in cornfields treated with and without this biological agent is needed to inform integrated pest management in corn. Fields receiving atoxigenic A. flavus applications of FourSureTM were compared to nearby control fields in three counties in corn production regions in eastern Texas. In each cornfield, 20 bee bowl traps were deployed along four equal transects located between corn rows, with contents of the bowls (i.e., bees) retrieved after 24 h. Eleven bee genera from four families were collected from cornfields, with only two honey bees collected and zero honey bees observed in transects. The sweat bee genus Agapostemon (primarily composed of the Texas striped sweat bee A. texanus) was most abundant in cornfields (44% of the total number of bees collected), followed by long-horned bees (Melissodes spp., 24%). The southernmost county (i.e., San Patricio) produced over 80% of the total number of bees collected. Bee numbers occurring in cornfields with applications of atoxigenic A. flavus applications were not significantly different from those of nearby control fields. Although not statistically significant, total numbers of bees tended to be lower in FourSure-treated fields than in control fields. More extensive research on bee abundances in relation to the effect of atoxigenic A. flavus is warranted.

Landscape context differentially drives diet breadth for two key pollinator species.

An animal's diet contributes to its survival and reproduction. Variation in diet can alter the structure of community-level consumer-resource networks, with implications for ecological function. However, much remains unknown about the underlying drivers of diet breadth. Here we use a network approach to understand how consumer diet changes in response to local and landscape context and how these patterns compare between closely-related consumer species. We conducted field surveys to build 36 quantitative plant-pollinator networks using observation-based and pollen-based records of visitation across the gulf-coast cotton growing region of Texas, US. We focused on two key cotton pollinator species in the region: the social European honey bee, Apis mellifera, and the solitary native long-horned bee, Melissodes tepaneca. We demonstrate that diet breadth is highly context-dependent. Specifically, local factors better explain patterns of diet than regional factors for both species, but A. mellifera and M. tepaneca respond to local factors with contrasting patterns. Despite being collected directly from cotton blooms, both species exhibit significant preferences for non-cotton pollen, indicating a propensity to spend substantial effort foraging on remnant vegetation despite the rarity of these patches in the intensely managed cotton agroecosystem. Overall, our results demonstrate that diet is highly context- and species-dependent and thus an understanding of both factors is key for evaluating the conservation of important cotton pollinators.

Solitary Floral Specialists Do Not Respond to Cryptic Flower-Occupying Predators

The impacts of predators on bee foraging behavior are varied, but have been suggested to depend on both the type of predator (namely their hunting strategy) and also risk assessment by the prey (i.e., ability to perceive predators and learn to avoid them). However, nearly all studies have explored these impacts using social bees, despite the fact that solitary bees are extremely diverse, often specialized in their floral interactions, and may exhibit different behaviors in response to flower-occupying predators. In this study, we examined foraging behaviors of wild solitary long-horned bees (Melissodes spp.) in response to a cryptic predator, the ambush bug (Phymata americana) on the bees’ primary floral host, the prairie sunflower (Helianthus petiolaris). We found sex-specific differences in foraging behaviors of bees, but little evidence that ambush bugs affected either pre-landing or post-landing foraging behaviors. Male bees visited flowers three times more often than females but female bees were five times more likely to land than males. Ambush bugs did not reduce visitation in either sex. Spectral analysis through a bee vision model indicated that ambush bug dorsal coloration was indistinguishable from the disc flowers of sunflowers, suggesting that ambush bugs are indeed cryptic and likely rarely detected by solitary bees. We discuss the implications of these findings for the perceived risk of predation in solitary bees and compare them to other studies of social bees.

Coastal soft cliff invertebrates are reliant upon dynamic coastal processes

Coastal soft cliffs in the UK support rich assemblages of invertebrates including species restricted to soft cliffs Howe (Br Wildl 4: 323–331, 2003). Recent analyses have identified a total of 29 species confined to coastal soft cliffs, with a further 78 species having a high degree of dependence (Howe et al. Br Wildl 19: 172–181, 2008). A handful of species once more widespread in the UK, both on the coast and inland, such as the Large Mason Bee Osmia xanthomelana and the Long-horned Bee Eucera longicornis, are now found only or mostly at soft cliff localities. Key habitats include bare sand or glacial till, extensive swards of leguminuous and ruderal plants and hydrological features including seepages, pools and reedbeds. Unhindered dynamic processes such as erosion and cliff failure and unimpeded drainage are critical to soft cliffs retaining their invertebrate interest. By far the richest sites for soft cliff invertebrates are on the Dorset and the Isle of Wight coasts, but other important localities include south Devon, the Llŷn coast in Gwynedd, north Norfolk, Yorkshire and the south Gower coast. The most obvious threats to soft cliff invertebrates are cliff-protection and stabilization schemes and drainage. However, agricultural improvement of cliff-top hinterlands at many sites restricts nesting and foraging activities to the immediate cliff slopes, and acts to fragment and isolate sections of soft cliff. More sympathetic management of these areas is needed to reconnect sites and their associated invertebrate populations, to reduce a dependence upon the cliff slope and to increase the availability of suitable nesting and foraging habitats.

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.

Scale-dependent shifts in the species composition of flower visitors with changing floral density

Responses of flower-visiting animals to floral density can alter interactions between plants, influencing a variety of biological processes, including plant population dynamics and the evolution of flowering phenology. Many studies have found effects of floral or plant density on pollinator visitation rates at patch scales, but little is known about responses of flower visitors to floral densities at larger scales. Here, I present data from an observational field study in which I measured the effects of floral density on visitation to the annual composite Holocarpha virgata at both patch (4 m(2)) and site (12.6 ha) spatial scales. The species composition of flower visitors changed with floral density, and did so in different ways at the two scales. At the site scale, average floral density within patches of H. virgata or within patches of all summer-flowering species combined had a significant positive effect on per-flowerhead visitation by the long-horned bee Melissodes lupina and no significant effects on visitation by any other taxa. At the patch scale, per-flowerhead visitation by honeybees significantly increased whereas visitation by M. lupina often decreased with increasing floral density. For both species, responses to patch-scale floral density were strongest when site-scale floral density was high. The scale-dependence of flower visitor responses to floral density and the interactions between site- and patch-scale effects of floral density observed in this study underscore the importance of improving our understanding of pollinators' responses to floral density at population scales.

Visual discrimination between two sexually deceptive Ophrys species by a bee pollinator

Almost all species of the orchid genus Ophrys are pollinated by sexual deception. The orchids mimic the sex pheromone of receptive female insects, mainly hymenopterans, in order to attract males seeking to copulate. Most Ophrys species have achromatic flowers, but some exhibit a coloured perianth and a bright, conspicuous labellum pattern. We recently showed that the pink perianth of Ophrys heldreichii flowers increases detectability by its pollinator, males of the long-horned bee Eucera berlandi. Here we tested the hypothesis that the bright, complex labellum pattern mimics the female of the pollinator to increase attractiveness toward males. In a dual-choice test we offered E. berlandi males an O. heldreichii flower and a flower from O. dictynnae, which also exhibits a pinkish perianth but no conspicuous labellum pattern. Both flowers were housed in UV-transmitting acrylic glass boxes to exclude olfactory signals. Males significantly preferred O. heldreichii to O. dictynnae flowers. In a second experiment, we replaced the perianth of both flowers with identical artificial perianths made from pink card, so that only the labellum differed between the two flower stimuli. Males then chose between both stimuli at random, suggesting that the presence of a labellum pattern does not affect their choice. Spectral measurements revealed higher colour contrast with the background of the perianth of O. heldreichii compared to O. dictynnae, but no difference in green receptor-specific contrast or brightness. Our results show that male choice is guided by the chromatic contrast of the perianth during the initial flower approach but is not affected by the presence of a labellum pattern. Instead, we hypothesise that the labellum pattern is involved in aversive learning during post-copulatory behaviour and used by the orchid as a strategy to increase outcrossing.

Why sexually deceptive orchids have colored flowers

Sexually deceptive orchids provide no reward to their pollinators. Instead, they mimic the sex pheromone of receptive insect females to attract males which pollinate the flowers in mating attempts. Nearly all species of the Mediterranean orchid genus Ophrys are sexually deceptive and pollinated by solitary bees and wasps. Due to the use of a highly specific olfactory communication channel most Ophrys species have, in contrast to food deceptive or rewarding orchids, an inconspicuous greenish perianth and a dark brownish labellum. However, some species possess a bright pink or white perianth, and the functional significant of such colour signals in the orchid-pollinator communication system is unknown. We recently showed that the pink perianth of Ophrys heldreichii increases the performance of its bee pollinator, males of the long-horned bee Eucera (Tetralonia) berlandi, to detect the flower at short-range. At great distances (>30cm) from the flower, male search behavior was found to be olfactory guided and unaffected by the spectral property of the perianth, i.e. chromatic and green receptor-specific contrast. However, in the near vicinity of the flower (<30cm), where spatial vision is sufficient to detect the flower, search time only correlated with the green receptor-specific contrast between the perianth and the background.

Floral colour signal increases short-range detectability of a sexually deceptive orchid to its bee pollinator

Orchids of the genus Ophrys are pollinated by males of solitary bees and wasps through sexual deception. The flowers mimic the behaviourally active compounds of the sex pheromone of receptive females and thus attract males that seek to copulate. Odour is the main attractant while visual stimuli have been assumed so far to play only a minor role. In contrast to most species of the genus, Heldreich's orchid Ophrys heldreichii, which is pollinated by males of the long-horned bee Tetralonia berlandi, possesses a bright pink perianth that appears conspicuous to a human observer. We investigated the role of this floral colour signal in pollinator attraction. We filmed approach flights of male bees to flowers in which we removed the original perianth and in which we substituted the perianth with an artificial one of a particular selected colour. At distances >30 cm, male search time correlated only with wind speed but not with the spectral parameters of the perianth, i.e. chromatic and green receptor-specific contrast. By contrast, in the close range (<30 cm), where the perianth subtends a visual angle of at least 5 deg. to the bee's eye, search time decreased with increasing green receptor contrast between perianth and background; however, no correlation with chromatic contrast or wind speed was found. Our results indicate that pollinators are first attracted by olfactory signals from a distance. Once in the vicinity of the flower where spatial vision of the males is sufficient, they are guided exclusively by vision. However, it can be expected that possession of a ;non-private' colour signal would increase the risk of pollen loss in sexually deceptive orchids by accidentally attracting non-specific flower visitors. We therefore discuss the occurrence of colour signals in the genus Ophrys in respect to the species-specific visual system of the pollinators.

A phylogeny of the oil bee tribe Ctenoplectrini (Hymenoptera: Anthophila) based on mitochondrial and nuclear data: Evidence for Early Eocene divergence and repeated out-of-Africa dispersal

The bee tribe Ctenoplectrini, with two genera, comprises nine species in tropical Africa and ten in Asia and Australia. Most of them collect floral oil, pollen, and nectar from Cucurbitaceae, but three species are thought to be cleptoparasites. The unusual morphology of Ctenoplectrini has made it difficult to infer their closest relatives, in turn preventing an understanding of these bees’ geographic and temporal origin. We used two mitochondrial and two nuclear markers (4741 nucleotides) generated for most of the species to test the monophyly of the tribe, its relationships to other Apidae, and its biogeographic history. Ctenoplectrini are strongly supported as monophyletic and closest to the Long-horned bees, Eucerini. The presumably cleptoparasitic species form a clade (Ctenoplectrina) that is sister to the remaining species (Ctenoplectra), confirming the independent evolution of cleptoparasitism in this tribe. Tree topology and molecular dating together suggest that Ctenoplectrini originated in Africa in the Early Eocene and that Ctenoplectra dispersed twice from Africa to Asia, sometime in the Late Eocene, 30–40my ago, from where one species reached the Australian continent via Indonesia and New Guinea in the mid-Miocene, c. 13my ago. Dry and cool mid-Miocene climates also coincide with the divergence between Ctenoplectra bequaerti from West Africa and Ctenoplectra terminalis from East and South Africa, perhaps related to fragmentation of the equatorial African rainforest belt.