Nocturnal Bee Research Articles

Unique morphological and morphometric traits of nocturnal bee antennae

Unique morphological and morphometric traits of nocturnal bee antennae

Low heat tolerance and high desiccation resistance in nocturnal bees and the implications for nocturnal pollination under climate change

Predicting insect responses to climate change is essential for preserving ecosystem services and biodiversity. Due to high daytime temperatures and low humidity levels, nocturnal insects are expected to have lower heat and desiccation tolerance compared to diurnal species. We estimated the lower (CTMin) and upper (CTMax) thermal limits of Megalopta, a group of neotropical, forest-dwelling bees. We calculated warming tolerance (WT) as a metric to assess vulnerability to global warming and measured survival rates during simulated heatwaves and desiccation stress events. We also assessed the impact of body size and reproductive status (ovary area) on bees’ thermal limits. Megalopta displayed lower CTMin, CTMax, and WTs than diurnal bees (stingless bees, orchid bees, and carpenter bees), but exhibited similar mortality during simulated heatwave and higher desiccation tolerance. CTMin increased with increasing body size across all bees but decreased with increasing body size and ovary area in Megalopta, suggesting a reproductive cost or differences in thermal environments. CTMax did not increase with increasing body size or ovary area. These results indicate a greater sensitivity of Megalopta to temperature than humidity and reinforce the idea that nocturnal insects are thermally constrained, which might threaten pollination services in nocturnal contexts during global warming.

Head geometric morphometrics as a reliable method to discriminate sexes and species of Megalopta, a nocturnal bee genus (Hymenoptera, Apoidea)

Head geometric morphometrics as a reliable method to discriminate sexes and species of Megalopta, a nocturnal bee genus (Hymenoptera, Apoidea)

Abundance, occurrence and time series: long-term monitoring of social insects in a tropical rainforest

The magnitude of worldwide insect decline is hotly debated, with multiple examples of stable or increasing insect populations. In addition, time series data for tropical insects are scarce, notably in rainforests where insect diversity is poorly known but reaches a peak. Despite social insects (ants, termites, bees and allies) being key organisms in these habitats, long-term monitoring data for these groups are crucially lacking. For many of these insects, the difficulty of locating nests in rainforests could be one reason. In this context, species occurrence in samples is often used as a surrogate for abundance to evaluate species distribution in space/time, but the loss of information is difficult to assess. In a tropical rainforest in Panama, we employed various sampling methods to examine the time series of seven insect assemblages with differing degrees of sociality: termite workers and soldiers, termite alates, bess beetles, litter ant workers, army ant alates, orchid bees, and nocturnal sweat bees. We used five community variables and six models related to occurrence and abundance, to test for significant trends in assemblages over a 13-year period (2009–2021). While assemblages of bess beetles increased, those of termite workers and soldiers, army ant alates, and orchid bees remained relatively stable. Termite alate, litter ant worker, and nocturnal bee assemblages showed signs of decline, demonstrating the need for monitoring distinct assemblages. Significant trends in generalized additive mixed models (GAMM) were observed in three out of five assemblages that could be tested. Our study indicates that trends in assemblages may be more informatively reported with abundance than with occurrence. We recommend (1) monitoring multiple insect assemblages as ecological indicators responsible for diverse ecosystem services; and (2) reporting species richness, changes in faunal composition, occurrence, and, when possible, using time-explicit analyses (such as GAMM models) for evaluating population trends over time.

Defensive shimmering responses in Apis dorsata are triggered by dark stimuli moving against a bright background.

Giant honeybees, including the open-nesting Asian giant honeybee Apis dorsata, display a spectacular collective defence behaviour - known as 'shimmering' - against predators, which is characterised by travelling waves generated by individual bees flipping their abdomens in a coordinated and sequential manner across the bee curtain. We examined whether shimmering is visually mediated by presenting moving stimuli of varying sizes and contrasts to the background (dark or light) in bright and dim ambient light conditions. Shimmering was strongest under bright ambient light, and its strength declined under dim light in this facultatively nocturnal bee. Apis dorsata shimmered only when presented with the darkest stimulus against a light background, but not when this condition was reversed (light stimulus against dark background). This response did not attenuate with repeated exposure to the stimuli, suggesting that shimmering behaviour does not undergo habituation. We suggest that this is an effective anti-predator strategy in open-nesting A. dorsata colonies which are exposed to high ambient light, as flying predators are more easily detected when they appear as dark moving objects against a bright sky. Moreover, the stimulus detection threshold (smallest visual angular size) is much smaller in this anti-predatory context (1.6-3.4deg) than in the context of foraging (5.7deg), indicating that ecological context affects the visual detection threshold.

Assessment of The Impact of Tiv Spiritual Weapons of Warfare on Countering Insecurity in Nigeria

This study considers the impact of Tiv spiritual weapons of warfare on countering insecurity in Nigeria. The study sampled 382 out of the population of 75,000. The snowball sampling technique was used in selecting the subjects for the study. Mean and standard deviation statistics was used in answering the research questions. The study found that there are different types of insecurities rampaging in Nigeria such as herdsmen terrorism and violence against Christian women and children, Boko Haram insurgency, armed robbery and kidnapping among others. This is due to the fact that there is failure of security agencies in the country in the intelligence services to contain the recurring security breaches and the judiciary’s compromise of cases that concern insecurity, among other factors. It is therefore, recommended that the security agents should adapt the use of Tiv spiritual weapons of warfare such as Ikyombo í Amazar (nocturnal atomic bomb), Ivyaan í Mbatugh(nocturnal arrow), Kper ú Mbatugh(nocturnal cast net), Iyou í Mbatugh(nocturnal bees), Gberkpugh ú Mbatugh(nocturnal bullet and cut proof) and Gberkpugh ú Tan(diurnal bullet and cut proof) for countering insecurity in Nigeria.

Floral Volatiles: A Promising Method to Access the Rare Nocturnal and Crepuscular Bees

Crepuscular and/or nocturnal bees fly during the dusk, the dawn or part of the night. Due to their short foraging time and sampling bias toward diurnal bees, nocturnal bees are rarely collected and poorly studied. So far, they have been mostly sampled with light and Malaise traps. However, synthetic chemical compounds resembling floral volatiles were recently found to be a promising alternative to attract these bees. By reviewing available literature and collecting original data, we present information on the attraction and sampling of nocturnal bees with scent-baited traps. Bees were actively captured with entomological nets while approaching to filter papers moistened with distinct chemical compound, or passively caught in bottles with scent baits left during the night. So far, all data available are from the Neotropics. Nocturnal bees belonging to three genera, i.e., Ptiloglossa, Megalopta, and Megommation were attracted to at least ten different synthetic compounds and mixtures thereof, identified from bouquets of flowers with nocturnal anthesis. Aromatic compounds, such as 2-phenyletanol, eugenol and methyl salicylate, and the monoterpenoid eucalyptol were the most successful in attracting nocturnal bees. We highlight the effectiveness of olfactory methods to survey crepuscular and nocturnal bees using chemical compounds typically reported as floral scent constituents, and the possibility to record olfactory preferences of each bee species to specific compounds. We suggest to include this method in apifauna surveys in order to improve our current knowledge on the diversity of nocturnal bees in different ecosystems.

Gongylolepis martiana, an Asteraceae pollinated by bats in the Amazon.

Most Asteraceae species are pollinated by insects, mainly bees and butterflies, although pollination by birds has been documented and pollination by bats has been suggested for some species. Here, we investigated the pollination of Gongylolepis martiana, a species supposedly pollinated by bats. We assessed floral traits and visitors in a population of G. martiana in the Brazilian Amazon, measuring pollen removal from anthers and deposition on stigmas by diurnal and nocturnal visitors. Florets opened at dusk and lasted for 4days, with the male phase starting on the first night and the female phase on the third night. Accumulated nectar per capitulum was 69.6μl per night and sugar concentration was 15%. Nectar-feeding bats and hummingbirds contacted the sexual parts, but pollen removal and deposition were greater throughout the night than during the day, when Meliponini bees considerably reduced pollen availability. Other nocturnal visitors of G. martiana were rare, including nocturnal bees and moths that foraged for pollen and nectar, respectively. Our results support that nectarivorous bats are the main pollinators of G. martiana, confirming Vogel's hypothesis of bat pollination in Asteraceae, particularly in the genus Gongylolepis. Since anthesis and each sexual floral phase started in the evening, nectarivorous bats and diurnal bees caused additive priority effects, preventing hummingbirds from being efficient pollinators. The high density of flowering individuals of G. martiana in patches from white-sand forests likely increases bat attraction, while the small amount of nectar per plant favours cross-pollination.

Nocturnal Bees as Crop Pollinators

Bees are typically diurnal but around 1% of described species have nocturnal activity. Nocturnal bees are still poorly studied due to bias towards studying diurnal insects. However, knowledge concerning their biology and role as crop pollinators has increased. We review the literature on nocturnal bees’ traits and their host plants, and assess the crop pollination effectiveness of this neglected group. Nocturnal bees have visual adaptations to cope with low light intensities, and floral scents are a key sensory cue used to find their host flowers. Nocturnal bees generally show high flower constancy, the ability to vibrate flowers, and high transfer rates of pollen grains to stigmas. The flowers visited by nocturnal bees range from small radial and zygomorphic flowers to large brush blossoms; moreover, they visit plants with different flowering strategies. Nocturnal bees are effective pollinators of regional fruit crops in Brazil, such as cambuci (Campomanesia phaea), guaraná (Paullinia cupana), cajá (Spondias mombin), and in North America of cultivated pumpkins (Cucurbita species). However, they most likely are pollinators of several other crops. Strategies to host high numbers of nocturnal bees around cropping areas should be taken, such as preserving adjacent native forests, restricting soil management, providing food resources beyond crop flowers, and avoiding light pollution.

Dorsal Landmark Navigation in a Neotropical Nocturnal Bee

Bees, ants and wasps are well known to visually navigate when traveling between their nests and foraging sites. When leaving their nest, landmarks in the vicinity are memorised and used upon return to locate the nest entrance 1-3 . The Neotropical nocturnal sweat bee Megalopta genalis navigates under the forest canopy at light intensities ten times dimmer than starlight. Despite these dim conditions, Megalopta is able to memorise visual landmarks around the nest entrance in the frontal visual field. Even though frontal landmarks can clearly be discerned by Megalopta, the visual feature of greatest contrast in the rainforest at night is actually the dark dorsal silhouette of the distant canopy against the brighter night sky. Several species of day-active ants, as well as a subsocial shield bug, use bright open gaps in the canopy as dorsal landmarks for short-range navigation while walking. Here we show that Megalopta is also able to distinguish dorsal landmarks, the first flying insect known with this capacity. Megalopta is able to discriminate between differently oriented dorsal black striped patterns, or an “artificial canopy” of black circles, and to use this information to locate its nest entrance. These results suggest that the local foliage patterns created by the canopy against the brighter sky could potentially provide the bee with reliable landmark information for navigation during foraging and homing at night.

Stark trade-offs and elegant solutions in arthropod visual systems.

Vision is one of the most important senses for humans and animals alike. Diverse elegant specializations have evolved among insects and other arthropods in response to specific visual challenges and ecological needs. These specializations are the subject of this Review, and they are best understood in light of the physical limitations of vision. For example, to achieve high spatial resolution, fine sampling in different directions is necessary, as demonstrated by the well-studied large eyes of dragonflies. However, it has recently been shown that a comparatively tiny robber fly (Holcocephala) has similarly high visual resolution in the frontal visual field, despite their eyes being a fraction of the size of those of dragonflies. Other visual specializations in arthropods include the ability to discern colors, which relies on parallel inputs that are tuned to spectral content. Color vision is important for detection of objects such as mates, flowers and oviposition sites, and is particularly well developed in butterflies, stomatopods and jumping spiders. Analogous to color vision, the visual systems of many arthropods are specialized for the detection of polarized light, which in addition to communication with conspecifics, can be used for orientation and navigation. For vision in low light, optical superposition compound eyes perform particularly well. Other modifications to maximize photon capture involve large lenses, stout photoreceptors and, as has been suggested for nocturnal bees, the neural pooling of information. Extreme adaptations even allow insects to see colors at very low light levels or to navigate using the Milky Way.

Nocturnal Bees Feed on Diurnal Leftovers and Pay the Price of Day – Night Lifestyle Transition

1. Bees exemplify flights under bright sunlight. A few species across bee families have evolved nocturnality, displaying remarkable adaptations to overcome limitations of their daylight-suited apposition eyes. Phase inversion to nocturnality in a minority of bees that co-exist with diurnal bees provide a unique opportunity to study ecological benefits that mediate total temporal niche shifts. While floral traits and sensory modalities associated with the evolution of classical nocturnal pollination syndromes, e.g. by bats and moths, are well-studied, nocturnality in bees represent a poorly understood, recently invaded, extreme niche. 2. To test the competitive release hypothesis, we examine how nocturnality shapes foraging by comparing pollen loads, nest pollen and flower visitation of sympatric nocturnal and diurnal carpenter bees. We predicted that nocturnal bees primarily use night-blooming flowers, show little/no resource overlap with diurnal species and competitive release favours night-time pollen collection for provisioning. 3. Contrarily, we found substantial resource overlap between nocturnal and diurnal bees. Flower opening times, floral longevity and plant abundance did not define nocturnal flower use. Smaller pollen loads on nocturnal foragers suggests subsistence on resource leftovers largely from diurnal flowers. Greater pollen types/diversity on nocturnal foragers indicates lower floral constancy compared to diurnal congenerics. Reduced activity during new moon compared to full moon suggests constraints to nocturnal foraging. 4. Invasion and sustenance within the nocturnal niche is characterised by: i)opportunistic foraging on residual resources as indicated by smaller pollen loads, extensive utilisation of day-blooming flowers and substantial overlap with diurnal bees, ii)generalisation at two levels – between and within foraging trips as indicated by lower floral constancy, iii)reduced foraging on darker nights, indicating visual constraints despite sensitive optics. This together with smaller populations and univoltine breeding in nocturnal compared to multivoltine diurnal counterparts, suggest that nocturnality imposes substantial fitness costs. 5. In conclusion, the evolution of nocturnality in bees is accompanied by resource generalisation instead of specialisation. Reduced floral constancy suggests differences in foraging strategies of nocturnal and diurnal bees which merits further investigation. The relative roles of competition, floral rewards and predators should be examined to fully understand the evolution and maintenance of nocturnality in bees.

Nocturnal bees exploit but do not pollinate flowers of a common bat-pollinated tree

Some species of bees restrict foraging to the twilight period before sunrise or after sunset. Among the plants sought by these nocturnal bees are species described as chiropterophilous, such as Caryocar brasiliense. The flowers of this species open in the evening and provide resources until dawn. We determined the pattern of flower visitation by nocturnal bees and their role in pollination and fruit set of C. brasiliense and evaluated its importance as floral resource for nocturnal bees. We analyzed the pollen composition of cell provisions of nocturnal bees of Ptiloglossa (Colletidae) and compared its scent with floral scent compounds of C. brasiliense. Moreover, we conducted a pollinator exclusion experiment to determine the contribution of nocturnal bees to its fruit set. Disregarding bats, Ptiloglossa latecalcarata and two species of Megalopta (Halictidae) were consistent nectar and pollen gathering visitors, along with some social diurnal bees. The visitor exclusion experiment revealed that bee visits do not result in fruit set, which only occurs through visits by bats. The flowers supply a significant amount of pollen for nocturnal bees, as demonstrated through pollen analysis of brood cells and scopa loads. This interaction, therefore, is only beneficial to the commensalist bees. The scent collected from brood cells was dominated by hexanoic acid and 1-hexanol and differed strongly from the floral scent of C. brasiliense. These results substantiate that bat-pollinated flowers are an important part of the food niche of nocturnal bees, which implies that they are sensorially equipped to recognize floral traits shaped by bats.

Light intensity regulates flower visitation in Neotropical nocturnal bees

The foraging activity of diurnal bees often relies on flower availability, light intensity and temperature. We do not know how nocturnal bees, which fly at night and twilight, cope with these factors, especially as light levels vary considerably from night to day and from night to night due to moon phase and cloud cover. Given that bee apposition compound eyes function at their limits in dim light, we expect a strong dependence of foraging activity on light intensity in nocturnal bees. Besides being limited by minimum light levels to forage, nocturnal bees should also avoid foraging at brighter intensities, which bring increased competition with other bees. We investigated how five factors (light intensity, flower availability, temperature, humidity, and wind) affect flower visitation by Neotropical nocturnal bees in cambuci (Campomanesia phaea, Myrtaceae). We counted visits per minute over 30 nights in 33 cambuci trees. Light intensity was the main variable explaining flower visitation of nocturnal bees, which peaked at intermediate light levels occurring 25 min before sunrise. The minimum light intensity threshold to visit flowers was 0.00024 cd/m2. Our results highlight the dependence of these nocturnal insects on adequate light levels to explore resources.

Nocturnal floral scent profiles of Myrtaceae fruit crops

Communication between plants and nocturnal pollinators in low light conditions is mainly guided by floral scents, which is well documented for plants pollinated by bats, moths, and beetles. Just recently, nocturnal bees have been added to the list of pollinators known to respond to floral scents of their host plants. Little is known about the floral scent chemistry of plants visited and pollinated by nocturnal bees. Among these plants are economically important fruit crops of the family Myrtaceae. We aimed to analyze the nocturnal floral scent profiles of 10 species of Myrtaceae (only diurnal P. cattleianum was sampled after sunrise) and address the following questions: i) What are the main floral scent compounds emitted by the species? ii) Are the floral scent profiles similar to those described for other species pollinated by nocturnal bees? Floral scents were collected by dynamic headspace and analyzed by GC-MS (gas chromatography - mass spectrometry). The total amount of scent trapped ranged from 74 ng/flower/hour for Syzygium malaccense to 7556 ng/flower/hour for Eugenia dysenterica. A total of 46 floral scent compounds were detected in the samples with the most abundant compounds being the aromatics benzaldehyde, benzyl alcohol, 2-phenylethanol, methyl salicylate, 2-phenylethyl acetate, and benzyl acetate; the aliphatic compound 1-octanol; and the monoterpene linalool. The different species exhibited different relative scent patterns. Overall, the nocturnal scents of the studied species of Myrtaceae are dominated by aromatic compounds, which is in contrast to the scent profiles described for other plants pollinated by nocturnal bees.

Nocturnal Bee Pollinators Are Attracted to Guarana Flowers by Their Scents.

Floral scent is an important component of the trait repertoire of flowering plants, which is used to attract and manipulate pollinators. Despite advances during the last decades about the chemicals released by flowers, there is still a large gap in our understanding of chemical communication between flowering plants and their pollinators. We analyzed floral scents of guarana (Paullinia cupana, Sapindaceae), an economically important plant of the Amazon, using chemical analytical approaches, and determined the attractiveness of the scent to its nocturnal bee pollinators using behavioral assays in the field. Pollen loads of attracted bees were also analyzed. Inflorescences of guarana emit strong scents, both during day and at night, with some semi-quantitative differences between day- and night-time scents. Synthetic scent mixtures containing some of the identified floral scent components, including the most abundant ones, i.e., linalool and (E)-β-ocimene, successfully attracted the nocturnal Megalopta bee pollinators. Pollen analyses revealed that many of the attracted bees had pollen grains from previous visits to guarana flowers on their bodies. Overall, our data show that guarana flowers attract nocturnal bee visitors by their strong scents and suggest that the chemical communication between this plant and its pollinators is a key component in crop production of this economically important plant species.

Pollination of Machaerium opacum (Fabaceae) by nocturnal and diurnal bees

With plants whose flowers open at night and stay open during the day, nocturnal pollinators may exploit floral resources before diurnal competitors. Moths, bats, and beetles are the most familiar nocturnal pollinators, whereas nocturnal bees as pollinators remain poorly understood. The common Cerrado tree Machaerium opacum (Fabaceae) has white and strongly scented melittophilous flowers, which first open at the night and remain open during the day and, thus, have the potential to be visited by both nocturnal and diurnal bees. We asked: (1) what is the plant’s breeding system? (2) when during the night do the flowers open? (3) what are the visual and olfactory floral cues? and (4) which nocturnal/diurnal bees visit and pollinate the flowers? We show that M. opacum is self-incompatible. Its flowers open synchronously at 03:30 h, produce nectar exclusively at night, and have an explosive mechanism of pollen presentation. The flowers have pure white petals, release strong scents during anthesis, and are pollinated by nocturnal and diurnal bees. We recorded four nocturnal and 17 diurnal species as flower visitors, with females of nocturnal species of Ptiloglossa (Colletidae) being the most abundant. After an initial pollen-releasing visit, only a minor amount of pollen remains in a flower. Several floral traits favor visits by nocturnal bees: (1) night-time flower opening, (2) nectar production at night, (3) almost complete pollen release during the first flower visit, and (4) pure white petals and strong odor production prior to sunrise, facilitating visual and olfactory detection of flowers when light is dim.

Effects of social organization and resource availability on brood parasitism in the facultatively social nocturnal bee Megalopta genalis

Understanding the ecological benefits that may select for the evolution of living in groups rather than solitarily is key to understanding the evolution of social cooperation. Defense against natural enemies, such as parasites and predators, is generally acknowledged to be such a benefit, but most studies focus only on predators. Among the bees, parasitism is a major source of brood mortality. Here we use the nocturnal, Neotropical, facultatively social bee Megalopta genalis (Halictidae) to directly compare parasitism rates between social and solitary nests at the same site during times of high and low resource availability. We focus on four parasites: one that eats some pollen but does not kill host offspring [the fly Fiebrigella sp (Chloropidae)] and three that kill host offspring (the beetle Macrosiagon gracilis (Rhipiphoridae), the wasp Lophostigma cincta (Mutillidae), and the congeneric bee M. Noctoraptor byroni). We found no difference in parasitism between social and solitary nests for the four parasites tested. Across all nests, 25–31% of brood cells were parasitized by Lophostigma sp., with parasitism increasing from the dry to wet season, although this seasonal effect was significant only for social nests. Only ~ 4% of brood cells were parasitized by one of the other three parasites, and M. byroni was only found in social host nests. Our data reveal that Megalopta have low rates of parasitism overall, and that this is not a function of social organization or resource availability. Limited nocturnal foraging time and foraging offset from the activity patterns of diurnal parasites may instead play a larger role in keeping parasitism rates low.

Thresholds and noise limitations of colour vision in dim light.

Colour discrimination is based on opponent photoreceptor interactions, and limited by receptor noise. In dim light, photon shot noise impairs colour vision, and in vertebrates, the absolute threshold of colour vision is set by dark noise in cones. Nocturnal insects (e.g. moths and nocturnal bees) and vertebrates lacking rods (geckos) have adaptations to reduce receptor noise and use chromatic vision even in very dim light. In contrast, vertebrates with duplex retinae use colour-blind rod vision when noisy cone signals become unreliable, and their transition from cone- to rod-based vision is marked by the Purkinje shift. Rod-cone interactions have not been shown to improve colour vision in dim light, but may contribute to colour vision in mesopic light intensities. Frogs and toads that have two types of rods use opponent signals from these rods to control phototaxis even at their visual threshold. However, for tasks such as prey or mate choice, their colour discrimination abilities fail at brighter light intensities, similar to other vertebrates, probably limited by the dark noise in cones.This article is part of the themed issue 'Vision in dim light'.

Pollination of Campomanesia phaea (Myrtaceae) by night-active bees: a new nocturnal pollination system mediated by floral scent.

Bees are the most important diurnal pollinators of angiosperms. In several groups of bees a nocturnal/crepuscular habit developed, yet little is known about their role in pollination and whether some plants are adapted specifically to these bees. We used a multidisciplinary approach to investigate the reproductive biology and to understand the role of nocturnal/crepuscular bees in pollination of Campomanesia phaea (Myrtaceae), popularly named cambuci. We studied the floral biology and breeding system of C.phaea. We collected the floral visitors and tested the pollinators' effectiveness. We also determined the floral scents released at night and during daytime, and studied behavioural responses of crepuscular/nocturnal bees towards these scents. The flowers of cambuci were self-incompatible and had pollen as the only resource for flower visitors. Anthesis lasted around 14h, beginning at 04:30h at night. The flowers released 14 volatile compounds, mainly aliphatic and aromatic compounds. We collected 52 species of floral visitors, mainly bees. Nocturnal and crepuscular bees (four species) were among the most frequent species and the only effective pollinators. In field bioassays performed at night, nocturnal/crepuscular bees were attracted by a synthetic scent blend consisting of the six most abundant compounds. This study describes the first scent-mediated pollination system between a plant and its nocturnal bee pollinators. Further, C.phaea has several floral traits that do not allow classification into other nocturnal pollination syndromes (e.g. pollinator attraction already before sunrise, with pollen as the only reward), instead it is a plant specifically adapted to nocturnal bees.