Today we have another combination story and biology lesson from Athayde Tonhasca Júnior, this time recounting how bumblebees can use electricity and the buzzing of their wings to find flowers and effect pollination. Athayde’s tale is indented, and photos, which you can enlarge by clicking, are attributed.

May the Force be with the bee

If we are asked how a bee finds a flower, we think of smells, colours, shapes and textures. These are important sensory signals, but there is another one whose relevance we are beginning to understand: electricity.

The platypus (Ornithorhynchus anatinus), a few fish and amphibians, and some ants, cockroaches, mosquitoes and fruit flies have the ability to detect external electric forces. But vertebrates need water as a conductive medium, while most insects respond only to unusually strong electric fields such as those generated by high voltage power lines. Bumble bees, however, have a sparking story to tell.

Now and then the thunder from a lightning bolt or the shock from a car door jolts us to the realisation that we are components of the Global atmospheric electrical circuit; our world is an immense electric motor. On a calm day, the air is positively charged, while the ground surface and any object connected to it – plants included – have a negative charge. So flowers have a slight negative charge in relation to the air around them. Flying insects experience different physical forces: as a bee buzzes along, electrons are stripped off its body by friction with the air, creating a surplus of positive charges. When the bee approaches a flower, she* attracts the negatively charged pollen grains. The grains stick to the bee, sometimes jumping from the flower even before the bee lands. These electrostatic forces are a great aid to pollination.

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*”She” because a worker honey bee is a sterile female. Apis mellifera sex has some quirks: embryos can develop as males through gene editing; populations of Cape honey bees (Apis mellifera capensis) reproduce without males; and some bacteria such as Wolbachia spp. change the sex of their arthropod hosts, including Hymenoptera (bees, wasps and ants). Nonetheless, their sex is typically binary, just as in Homo sapiens.

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Fig. 1. An electrifying encounter: a positively charged bee approaches a negatively charged flower © Hooven et al., 2019. Molecules 24, 4458.

Fig. 2. Pollen clinging to a bee © Ragesoss, Wikimedia Commons.

But flower power reaches shocking levels for the buff-tailed bumble bee (Bombus terrestris), and probably for other bumble bees as well: they are able to sense the weak electric field around a flower. No one knows exactly how they do it, but mechanoreceptive hairs must be involved. These special hairs are innervated at their base, so they detect mechanical stimuli such as air movement and low frequency sounds. Apparently, the flower’s electrical field moves the mechanoreceptive hairs of an approaching bee, similar to the way a wiped rubber balloon makes your hair stand on end. This hair movement is processed by the bee’s central nervous system and gives information about the shape of the electric field. It works just like Uri Geller’s mystical aura, except that the bee is not a fraud and its powers are not mystical.

Fig. 3. A buff-tailed bumble bee worker with a transponder attached to its back to track it with radar © Meadows, 2012. PLoS Biol 10(9): e1001391.

Fig. 4. Hairs provide thermal insulation, collect pollen and help bees sense air motion, sounds and electricity © Kevin Mackenzie, University of Aberdeen. Attribution 4.0 International (CC BY 4.0).

But bumble bees’ capacity to detect electric forces may go beyond recognising flowers’ sizes and shapes: they could use the information to maximise foraging trips. Once a positively charged bee lands, the flower’s electric field changes and doesn’t go back to normal for about two minutes after the bee leaves. Researchers believe that an altered field warns the next bee that the flower is temporarily depleted of nectar; it’s like turning off a ‘we are open’ neon sign. So the next bee may as well buzz off to another flower with sufficient negative charge and a decent volume of nectar.

Bees and other insects detect ultraviolet and polarized light, and use magnetic fields for navigation. Sensing electricity is one more way their world is experienced differently from ours. And the relationship of bees with physics has other important implications, some of which affect our food supplies.

For most species of flowering plants, fertilization depends on the transfer of pollen from the male anthers of one flower to the female stigma of another. For the majority of those flowers, pollen is released through the splitting open (dehiscence is the technical term for it) of mature anthers. But for approximately 6% of the world’s flowering plants, pollen is kept locked inside non-dehiscent anthers and accessed only through small openings – pores or slits – in their extremities. We refer to them as poricidal anthers.

Fig. 5. Left: stamens, consisting of filaments and anthers. André Karwath, Wikimedia Commons. Most flowers release pollen by the splitting of the anthers along a line of weakness (top right); some only do it through a small hole or pore (bottom right).

Sometimes the whole flower has a poricidal arrangement, as it is the case for the tomato and related plants (Solanum spp.). Pollen is concealed inside a cone-shaped cluster of fused stamens and can only be released though a pore at the tip. Botanist say these flowers have a solanoid shape, after the name of the plant genus.

Fig 6. Solanoid-shaped tomato flowers © Muffet, Wikimedia Commons.

Extracting pollen from poricidal structures is not easy, but some bees know a way to do it.

A bee lands on one of these flowers, bites an anther and curls her body around it. She then lets out bursts of fast contractions and relaxations of her thoracic muscles – those muscles used for flying, but here the wings remain still. The contractions produce cyclical deformations of her thorax that last from fractions of a second to a few seconds: think of a body builder flexing his pectoral muscles really, really fast. These movements generate vibrations that are transmitted to the anther, causing pollen grains to fall though the apical pores and land on the bee’s body, adhering to it with the aid of electrostatic forces.

Fig. 7. A bee engaged in buzz pollination © Bob Peterson, Wikimedia Commons.

This head-banging pollen-harvesting manoeuvre generates a high-pitched buzz, hence it is known as ‘buzz pollination’; or as ‘sonication’ in technical reports. A physicist or an engineer could point out that this mechanism is not strictly sonication because it’s not sound that agitates and extracts pollen, rather the bee’s vibrations on the flower. But ‘sonication’ is the term commonly adopted, so we will keep it. Bumble bees (Bombus spp.), carpenter bees (Xylocopa spp.), and some other bees can buzz pollinate: honey bees (Apis spp.) and most leafcutter bees (Megachile spp.) cannot. And apparently only females know the trick; males have never been recorded buzz pollinating. Watch the whole sequence of events here (buzz pollination from 0:49) and here.

Plants with poricidal floral morphology are distributed across at least 80 angiosperm families, which suggests that buzz pollination has evolved independently many times. This has probably been helped by bees’ readiness to buzz for other reasons such as warning enemies, compacting nest materials, or cooling/warming their nests by beating their wings.

“Buzz-pollination syndrome”, the name given for this plant-bee association, is not just a biological curiosity. It makes a huge difference for crops such as tomatoes, raspberries, cranberries, blueberries, aubergines, kiwis and chili peppers. These plants don’t necessarily need buzz pollination to reproduce, but they produce more and better fruit if they are buzzed because more pollen is transferred and more ovules are fertilised.

In the late 1980s, Belgian and Dutch companies developed techniques to rear at a large scale the buff-tailed bumble bee, the ultimate buzz pollinator. Local producers of greenhouse tomatoes began replacing costly mechanical pollinators with boxes containing bumble bee hives, and a global, multi-million pound industry was born. Today, all ordinary tomatoes bought in a European supermarket have matured with the help of commercially reared bumble bees (they also transmit diseases to wild bees, but that’s a story for another time).

Fig. 8. A commercial bumble bee hive used in greenhouses © Elaine Evans, The Sustainable Agriculture Research and Education.

We may see pollination as a harmonious relationship where plant and insect go out of their way to help each other, but this is mistakenly romantic. A bee aims to take all the flower’s pollen: pollination happens because a few grains are dropped or rubbed off by accident. And a plant produces as little nectar and pollen as necessary to entice a flower visit. So the association between pollinators and flowers is best described as a mutual exploitation.

Buzz pollination fits nicely into this scenario. Poricidal anthers prevent excessive pollen expenditure by rewarding only a few specialist pollen gatherers, which increases the chance of pollination. Plants with poricidal structures typically secrete little or no nectar but their pollen is rich in protein, which convinces a bee to go to the trouble of buzzing to gain a small dose of the yellow stuff. It’s a clever and efficient trade agreement in the pollinators’ world.

Today we have another history/natural history/general interest contribution from reader Athayde Tonhasca Junior. His notes are indented, and click on the photos to enlarge them.

If you walk into a British supermarket and pick up a tin of Lyle’s Golden Syrup or Black Treacle (these are by-products of sugar refining processes, similar to corn syrup and molasses), you will notice one of the strangest logos for a food product: a dead lion surrounded by a swarm of bees above the slogan ‘Out of the strong came forth sweetness’.

Lyle’s Black Treacle:

The image and text are based on the Biblical tale in which Samson kills a lion to find a honeycomb inside it. This unexpected discovery led Samson to write a riddle: ‘Out of the eater came forth meat and out of the strong came forth sweetness’. Meaning: from the carcass of a lion (the eater and the strong), Samson had meat and honey (sweetness). The story impressed the staunch Presbyterian Abram Lyle (1820-1891), businessman and founder of the sugar refinery Abram Lyle & Sons. And so one of Britain’s oldest brands was born: the logo hasn’t changed much since 1885.

But the yarn about dead animals and bees is older than Samson’s adventure. The Greeks, the Romans and other Mediterranean peoples believed that honey bees originated spontaneously from animal carcasses, primarily of oxen. The Greeks had a name for this miracle: bugonia, from bous (ox) and gon (generation). The Roman poet Virgil (70-19 BC) told the story of a farmer, who in want of bees, slaughtered an ox and waited for a new swarm. Bugonia inspired Shakespeare as well: ‘Tis seldom when the bee doth leave her comb, in the dead carrion’ (Henry IV).

Bugonia, unknown author, 1517:

But the belief in carcass apiculture suffered a fatal blow in 1668, when the Italian physician, naturalist, biologist and poet Francesco Redi (1626-1697) published Esperienze Intorno alla Generazione degl’Insetti (Experiments on the generation of insects). By comparing covered and uncovered meat-filled glass containers and observing the presence or absence of flies and maggots, Redi put an end to the idea of spontaneous generation.

Bugonia was dead, but the recurrent reports of bees swarming around carcasses, just like in Lyle’s logo, still required explanation. Enter diplomat and entomologist Baron Karl-Robert von Osten-Sacken (1828-1906), who, despite his Teutonic name, was Russian. The Baron suggested that the ‘bees’ found around dead animals were in fact flies: not the expected carrion-seeking blow flies and blue bottles, but the drone fly, Eristalis tenax.

The name ‘drone fly’ comes from its resemblance, in appearance and behaviour, to honey bees. The adults feed on pollen, especially from yellow flowers such as dandelions, and are known to pollinate various crops. The larva has a long ‘tail’, which is a specialized respiratory structure that works as a snorkel, allowing the insect to breathe air from the surface when submerged in liquids. This respiratory appendage gives the larva its common name: the rat-tailed maggot.

A male drone fly. Like many fly species, males have larger eyes that almost touch, while female eyes are spaced apart © Sandy Rae, Wikimedia Commons.

A drone fly larva, or rat-tailed maggot © Obsidian Soul, Wikimedia Commons.

In his 1894 publication ‘On the oxen-born bees of the Ancients (bugonia) and their relation to Eristalis tenax, a two-winged insect’, von Osten-Sacken explained the bugonia phenomenon as this: ‘The original cause of this delusion lies in the fact that a very common fly, scientifically called Eristalis tenax (popularly the drone-fly), lays its eggs upon carcasses of animals, that its larvae develop in the putrescent mass, and finally change into a swarm of flies which, in their shape, hairy clothing and colour, look exactly like bees, although they belong to a totally different order of insects.’

The Baron was close: the female drone fly does not lay her eggs on carcasses, but on the exudates and foul water accumulated around them. Other contaminated water sources would do, such as sewage, manure lagoons, holding pits in livestock areas, ditches and wet silage.

Hence an entomological/historical mystery may have been solved.

Drone flies are not the only insects interested in a dead lion: blow flies of the genus Lucilia may get to it first – or to a dead bird or small mammal in your neighbourhood. You will certainly have seen these shiny, metallic green flies, known as green bottles, in your garden or around your bins. They comprise several species that are difficult to tell apart.

A female green bottle fly.

Female green bottle flies use their powerful sense of smell to track minute volumes of sulphur volatiles released by recently deceased animals. Once a fly finds a corpse, sometimes within minutes of death, she lays 150 to 200 eggs on it. The eggs quickly hatch into maggots, which feed on the rotting flesh. After about ten days, they leave the body and pupate in the soil nearby.

Gross, you say? Well, green bottle flies help decompose carcasses, accelerating the release of organic matter and nutrients into the ecosystem. Without them and other scavenging insects such as flesh flies and carrion beetles, decomposition by microorganisms would take much longer, and rotting carcasses would accumulate in the landscape. Alas, these flies can lay their eggs on live bodies as well. The common green bottle fly Lucillia sericata is a serious pest of sheep, causing significant expenses for farmers.

However, green bottle flies are not all death and pestilence. Because their maggots preferentially consume dead tissue, they have been used for the treatment of non-healing wounds in people and animals. Maggot therapy has been known since 1557 when Ambroise Paré (c. 1510-1590), the Chief Surgeon of King Charles IX of France, described a soldier with a deep head wound filled with a ‘great number of worms’, and noted that the patient ‘recovered beyond all men’s expectation’. This unusual but effective treatment saved many lives before antibiotics become widely available, and the therapy is experiencing a comeback because of antibiotic resistance. Disinfected L. sericata maggots are placed in a diabetic ulcer, bedsore or other chronic wound, where they eat the necrotic tissue and produce antimicrobial enzymes that prevent infections, thus speeding the growth of new tissue.

Maggot debridement (the removal of necrotic tissue to help a wound heal) on a diabetic foot © Alexsey Nosenko/Maggot Medicine, Wikimedia Commons

Wound healing is not the only service provided by L. sericata. This species is a good pollinator of crops that produce few flowers or little pollen such as cauliflower, cabbage, lettuce, carrot, onion, leek, and asparagus; so much so that this fly is commercially available to complement the pollination by bees in glasshouses. Not so bad for those green creatures buzzing around your rubbish!

Because drone flies and green bottles are dependent on dead bodies, they are important aids to forensic science. By noting the flies’ life stage, criminal investigators can determine a person’s time of death, and the presence or absence of flies in certain environments can be an indication of tampering with the body: drone flies for example are indicators of partially submerged cadavers.

Forensic entomology students learning the ropes © UC Riverside.

Shortly after an animal expires, its body starts releasing the scents of decay. Thanks to their sensitive antennae, sexton beetles such as Nicrophorus vespilloides can locate a corpse within an hour of death and from as far away as 3 km. The first male-female pair to arrive examines it to assess its size; bodies too big to be handled are rejected. If the ground is unsuitable for digging, they drag the body to a better location, all the while fencing off late arrivals and competitors.

A common sexton beetle, Nicrophorus vespilloides © Holger Gröschl, Wikimedia Commons.

The beetles loosen the soil with their heads and shove it aside, gradually constructing a burial chamber that eventually sinks the carcass into the ground, a process that may take up to 8 hours. After burial, the beetles strip away any fur or feathers and shape the flesh into a compact ball, dousing it with secretions that act as anti-bacterial agents to slow down decomposition. The female then lays her eggs in the soil nearby. Watch sexton beetles in action here and here.

Two common sexton beetles in a dead rodent caught in a mousetrap © Calle Eklund, Wikimedia Commons.

Until they are about three days old, sexton beetle larvae beg for food by pressing against the adult’s jaws, which stimulates regurgitation – a behaviour normally associated with birds and their nestlings. Afterwards the larvae feed directly on the carcass, but they are cared for by their parents throughout their development. This is a rare and highly developed behaviour in insects, normally found in social bees, wasps, ants, and termites. But it’s not all love and care in the life of a young sexton beetle; if the adults sense that the brood is too big or the carcass is too small, some of the smaller larvae are eaten, so that the remaining ones will have a sufficient food supply.

A female N. vespilloides feeds her begging young © Allen J. Moore, Nature Communications 6: 8449.

These complex interactions between parents and offspring represent the highest degree of sociality among Coleoptera, and that’s why sexton beetles are considered to have attained the level of ‘subsocial’ on insects’ sociality spectrum. And recently, a new twist has been revealed in their intricate lives.

A female dedicates her time and energy to the offspring. The male however may have other ideas thanks to sexual competition; he may be driven to pester her for sex to guarantee paternity because given the chance, other males will have a go with the busy female. She has a chemical solution for this harassment problem: during early stages of larval growth, she releases methyl geranate, which has anti-aphrodisiac properties and inhibits the mating instinct of males.

So there you have it: sexton beetles have created the first anti-Viagra.

If you bump into a dead lion or another cadaver, you may pause to brood over life and mortality. But although that carcass was the end of the line for one life, by no means was it the end of the line for life. Dead animals (and dung as well) are valuable resources, full of complex proteins, carbohydrates, fats and sugars. And many creatures are ready to exploit the life opportunities offered by a corpse.