Reluctant givers and industrious takers

By Athayde Tonhasca

For bees, pollen is an indispensable source of protein for egg production and larval development. So if they had it their way, bees would scoop up every pollen grain from a flower. And they are good at it, taking 95 to 99% of the powdery stuff back to their nests. The ‘wasted’ 1 to 5% of pollen that bees accidentally drop off or is left clinging to the bees’ hairs, is all a plant has for pollination.

Bees such as honey bees (Apis spp.) and bumble bees (Bombus spp.) carry almost all the pollen they gather in their corbiculae, or pollen baskets. From the Latin diminutive of corbis (basket), the corbicula is a shallow leg cavity surrounded by a fringe of elongated setae (‘hairs’). These bees, unsurprisingly called corbiculate bees, moisten the pollen with regurgitated nectar and saliva, so that it can be bundled up nicely for transport and easily unloaded once bees are back at their nests. 

A European honey bee’s pollen basket © Gilles San Martin, Wikimedia Commons.

A corbiculate bee grooms herself regularly to remove stray pollen grains stuck to her body: most of them will be scooped up and stored securely © Ragesoss, Wikimedia Commons.

Other bees carry pollen attached to their scopa (Latin for ‘broom’), which is an area of dense, stiff hairs on the hind legs (typically in the families Halictidae and Andrenidae) or on the underside of the abdomen (mostly in the family Megachilidae). These non-corbiculate bees are not as tidy as their corbiculate counterparts: they do not wet and compress the pollen, but instead take it away just like dust particles clinging to the bristles of a brush or a broom.

The scopa of a megachilid or leaf-cutter bee © Pollinator, Wikimedia Commons.

Transporting pollen on the corbiculae or scopa makes a world of difference for pollination. Pollen tightly packed in the corbiculae is not easily stripped off by floral structures when the bee visits another plant, and it quickly loses its reproductive viability because it has been wet. Pollen on a scopa is kept dry and loosely attached to the bee, so it has a greater probability of being dislodged and resulting in plant fertilisation. 

A load of pollen in a bumble bee’s pollen basket © Tony Wills, Wikimedia Commons, and a chocolate mining bee (Andrena scotica) with pollen loosely attached to its legs.

Regardless of how pollen is hauled away, bees’ efficiency puts plants in a jam. They need flower visitors for sexual reproduction, but the greedy blighters want it all for themselves. Pollen is metabolically expensive, so a plant can’t afford to produce lots of it and then lose most to palynivores (pollen eaters). But if it produces too little, bees may not be interested in dropping by.

To deal with this dilemma, plants have evolved strategies to keep visitors coming and at the same time not making it easy for them, thus minimising pollen profligacy. One cunning way to do this is to interfere with bees’ ability to groom themselves, so that more pollen grains are likely to be missed and end up on a receptive flower. To do this, there’s nothing better than nototribic flowers, which are built with an elaborate lever mechanism that makes stamens and style touch the dorsal surface of a visiting insect. This device is common in sage, mint and rosemary plants (family Lamiaceae), and in figworts (family Scrophulariaceae).

When a male Anthophora dufourii probes a Salvia hierosolymitana flower for nectar, its stamens are lowered to deposit pollen on the bee’s back © Gideon Pisanty, Wikimedia Commons.

Bees use their front legs to wipe their heads and antenna, and their middle and hind legs to clean their thoraxes and abdomens – you may have watched a bee or other insect doing these cleaning manoeuvres. But the space between their wings is a blind spot: think about an itch right between your shoulder blades, and you will understand the bee’s pickle. The pollen grains deposited on this hard-to-reach area are likely to escape grooming efforts and be taken to another flower.  

Pollen of meadow clary (Salvia pratensis) seen under UV light on the back of B. terrestris © Koch et al., 2017.

Some flowers hide pollen at the bottom of their corollas, and visitors such as the fork-tailed flower bee (Anthophora furcata) must creep into these narrow, tubular structures that don’t allow much moving about. The bee vibrates her flight muscles to release the pollen, which gets attached to her head. She pulls out of the flower and scoops up the pollen with her front legs, but not all of it. Some grains become stuck to the thick, curved hairs sticking out between her antennae; these grains could end up on another flower. 

A fork-tailed flower bee has to use her head – literally – to pollinate © Dick Belgers, Wikimedia Commons.

The common hollyhock (Alcea rosea) and other mallows (family Malvaceae) use a different tactic: they induce some bees to be less efficient gatherers thanks to their echinate pollen. Besides being prickly (echinate: covered with spines or bristles), these pollen grains are relatively large, thus difficult to handle and to mould into neat pellets. These features constitute a headache for corbiculate bees, the proficient packers, but are less of a problem for sloppy pollen harvesters such as solitary bees. As a result, more pollen grains are likely to be dislodged from bees who bother visiting these plants, increasing their chances of pollination. 

Echinate pollen grains from Malvaceae and other species © Konzmann et al. 2019.

Plants have developed other adaptations to minimise pollen harvesting, such as complex flower structures or progressive pollen release to force pollinators to make repeated visits. Some species hide pollen inside poricidal anthers, others produce indigestible or even toxic pollen so that only a few specialised pollinators can get to it; the palynivore hoi polloi is kept at bay. Many plants such as orchids are downright cheats: they lure pollinators with scent or visual mimicry but do not give away any nectar or pollen in return. 

All these adaptations demonstrate that pollination is a negotiation between parties with conflicting interests. There is nothing altruistic here, bees and flowers are taking advantage of each other in an evolutionary give and take. Granted, this mutual exploitation has been fine-tuned in order to avoid disastrous imbalances. Plants can’t afford giving away too much pollen but can’t risk being too stingy; bees would take all the pollen they could handle, but settle for what’s available as long it’s worth their time and energy. Overly parsimonious plants and overly rapacious bees would collapse the relationship. Every plant-pollinator combination is an example of a mutually beneficial compromise; it’s natural selection as its best.

A sloppy but efficient pollinator

By Athayde Tonhasca

We hear a lot about the pollination services provided by the European honey bee (Apis mellifera), so you may be surprised to know this bee is not that competent at its job. A honey bee moistens the pollen she collects and carries it tightly packed on her corbicula, or pollen baskets, so pollen grains are not easily dislodged when the bee visits another flower. Moreover, honey bees learn quickly to collect nectar with minimal contact with the flower’s anthers, so reducing the chances of pollen transfer. They are also good at flower constancy (the trait of visiting the same type of flower over and over), which is not good for plants that need cross-pollination between different varieties, such as apples. Thus, paradoxically, honey bees’ efficiency as food collectors reduces their efficiency as pollinators. These shortcomings are offset by the huge numbers of bee workers per hive and the fact that they are so amenable to management.

In comparison with the tidy honey bee, the red mason bee (Osmia bicornis) is a messy flower visitor. Females have low flower constancy, flying all over the place, and carry dry pollen loosely attached to their scopa (a mass of hairs under the abdomen). This means that pollen grains have a greater chance of becoming detached from the bees’ bodies and ending up on a flower’s stigma.

A red mason bee with her scopa loaded with pollen © Jeremy Early, Nature Conservation Imaging

What’s more, the red mason is one the most polylectic bees in Europe, that is, it collects pollen from a variety of flowers from unrelated species: 18 plant families altogether, including willows (Salix spp.), maples (Acer spp.), birch (Betula spp.), oaks (Quercus spp.) and several fruit trees in the family Rosaceae such as apples, pears, plums, cherries and peaches. Unsurprisingly, this bee is an excellent orchard pollinator; 500 or so female red masons can pollinate as many trees as 2-4 honey bee colonies. 

Like other Osmia species, the red mason is a cavity-nesting bee; it makes itself at home in preexisting holes and fissures in soil banks or dead wood, abandoned insect burrows, hollow stems, or cracks and holes in walls – which explains the common name, ‘the mason bee’. It may also excavate soft mortar, hence the reason for another common name: ‘the mortar bee.’ The red mason readily occupies man-made structures such as ventilation bricks, the space beneath roof tiles, even inside door locks. So this bee is the most likely tenant of bee houses.

Once a female occupies a cavity, she will construct a series of compartments (brood cells) and stock them with pollen as food for her offspring. She will then close the nest entrance with a mud plug. But she’s not done once the nest is finished: if conditions are right, she may build another six nests before the season is over. The larvae will eat the pollen and emerge as adults the following year to start the cycle again. See red mason bees in action here.

A session of a mason bee nest. Each cell contains one egg and a provision of pollen 

Mason bees tend to nest close to each other in aggregations of 50 to 250 females. And they are diligent pollinators, as demonstrated by these facts and figures:

• A female bee may construct 16 cells per nest, 1 cell/day.
• She will fly 300-400 m on average, up to 600 m, in search of flowers.
• Nineteen foraging trips are needed to collect the pollen and nectar for each cell.
• Her pollen load weighs 100-250 mg, up to 300 mg.
• She may visit 75 flowers each trip, up to 25 flowers/min, and she will stock up each cell in about 3.5 h.
• A cell with an egg that will develop into a female bee may contain 8 million grains of pollen. Fewer for male bees (they need less food): 4.6 million.

This hardworking bee is good news for wild flowers, and also for crop production. The red mason is an effective pollinator of rapeseed oil and a number of crops grown under polytunnels and glasshouses, such as strawberries and raspberries. Other mason bees have been managed as orchard pollinators in Japan and USA for many years; there is growing evidence that the red mason can play a similar role in orchards in Britain and other European countries.

A female red mason bee and sealed nests in a bee house

The red mason bee is common throughout most of the UK from late March to June/July. During this short time as an imago (the adult stage), this bee will contribute to the pollination of countless wild flowers, crops and fruit trees. The red mason bee deserves to share the spotlight with the honey bee.     

Changes in the menu

By Athayde Tonhasca

If in a perambulation outdoors you spot a bee slipping into a hole in the ground, chances are it’s an Andrena species. Many bees are fossorial (from the Latin fossor for ‘digger’, it refers to species that excavate the soil and spend most of their life underground), but Andrena is the most common group by far. With 68 species recorded in Britain and around 1,400 described species worldwide, this is one the largest animal genera. 

Like all mining bees, Andrena species are solitary: a female builds her own nest chambers in which she stocks pollen and lays her eggs. Although each bee minds her own business, many species are communal nesters, sometimes forming aggregations thousand strong. Some species like the chocolate mining bee (Andrena scotica) use a common nest entrance, giving the impression of social behaviour. But once beyond the front door, each bee digs her own side tunnel and provisions her own chambers.

A group of chocolate mining bees hanging around a communal nest entrance in a wall in Perth 

These bee concentrations frighten some people. Beekeepers and council officers have been summoned to deal with ‘swarms,’ only to find the comings and goings of mining bees. Worse, people afraid of being stung or concerned about damage to buildings or lawns have wiped out whole colonies with insecticides. But these citizens are mistaken on both counts. Solitary bees are docile and never go out of their way to attack people or animals; besides, their sting is too weak to penetrate human skin. And their nesting galleries are temporary and too small to cause any damage.

Many bee species collect pollen on their corbiculae (pollen baskets) or scopa, which is an area of dense, stiff hairs on their hind legs or on the underside of their abdomen. Female Andrena bees have an additional collecting apparatus: a large brush of curled hairs on the hind legs called floccus. So these bees manage to carry large loads of pollen, which increases the chances of pollination. Because of their diversity, abundance and efficiency, Andrena bees must contribute to the pollination of crops, trees and wild flowers, although we don’t have detailed information about these services.

A grey-backed mining bee (Andrena vaga) loaded with pollen © Agroscience RLP, Wikipedia Creative Commons

As Andrena bees and other pollinators depend on flowers, they are particularly vulnerable to losses or impoverishment of plant biodiversity. So they were caught in the environmental maelstrom unleashed by the Second World War.

Under the trauma of shortages and threat of famine, the UK government was determined to make the country self-sufficient in food production. In came the 1947 Agriculture Act, which changed Britain forever. The subsequent rapid agricultural intensification led to increased efficiency and production, but there was a price to pay: modern farming practices severely reduced the areas of natural and semi-natural habitats, and depleted biodiversity.

A modern farm offers few opportunities to pollinators © European Environment Agency

Fortuitous museum collections offered an exceptional opportunity to gauge the effects of these historical habitat changes on the British Andrena fauna. By comparing pollen grains attached to Andrena bees collected between 1941 and 1949 with bees collected between 1985 and 2016, Wood & Roberts (Biological Conservation 215: 72–80) obtained a glimpse of bee diets before and after the onset of agricultural intensification.

Pollen loads from both periods revealed one particularly significant shift: a move from Rosaceae family (hawthorns, cherries, crab apple) to oilseed rape (Brassica napus). These results were not surprising: hedgerows have been cut down for the sake of improving farming operations, so many woody Rosaceae plants have disappeared from the landscape. At the same time, oilseed rape boomed: British production has risen from a few thousand tonnes in the 1970s to a couple of million today. Worldwide production has increased six-fold between 1975 and 2007, and this crop has become the third largest source of vegetable oil in the world.

Change in the offerings: from a hawthorn hedge to an oilseed rape field © David Hawgood (L) and Nas2, Wikipedia Creative Commons

The change from small fields criss-crossed by hedgerows and uncultivated plants to monotonous oilseed rape crops is likely to affect Andrena bees in different degrees. Most species are polylectic, that is, they collect pollen from various types of flowers. But some species are oligolectic: they collect pollen from a few related plant species. Pollen specialisation is an obvious problem when the landscape is awash with the wrong type of flowers, but hard data are scant. Landscape simplification may have contributed to the decline of the blackthorn mining bee (Andrena varians), which collects pollen mostly from early-flowering blackthorn and hawthorn. Other species may have been hit as well with the loss of swathes of uncultivated plants. So for example the decline of the grey-banded mining bee (Andrena denticulata) may be linked to lower availability of weedy species from the Asteraceae family such as daisies and aster, which are the bee’s main pollen sources. 

Habitat loss has significantly affected wild bees in North America and Western Europe – and probably elsewhere too. Reversing the trend by diversifying agricultural landscapes and preserving the remaining natural habitats are the best means to mitigate the effects of the post-war ‘green revolution’ and safeguard the pollination services provided by Andrena and other bees.

Two bees punished by agricultural changes: the blackthorn (L) and grey-banded mining bees © Aiwok (L), and Sandy Rae, Wikipedia Creative Commons

Pollination, a game of hide and seek

By Athayde Tonhasca

For bees, pollen is an indispensable source of protein for egg production and larval development. So if a bee had it her way, she would scoop up every pollen grain from a flower. And she’s good at it, storing pollen securely on specialised transport structures, usually on her legs or under her abdomen. She also grooms herself regularly to remove stray pollen grains stuck to her body. As a result of this meticulous work, some bees take about 99% of the powdery stuff back to their nests. The ‘wasted’ 1%, which accidentally drops off or is left clinging to the bees’ hairs, is all a plant has for pollination. 

A bee covered in pollen grains: most of them will be scooped up by the bee © Ragesoss, Wikipedia Creative Commons

Bees’ efficiency puts plants in a jam. They need flower visitors to transport pollen and for sexual reproduction, but the greedy blighters want it all for themselves. Pollen is metabolically expensive, so a plant can’t afford to produce lots of it and then lose most to palynivores (pollen eaters). But if it produces too little, bees may not be interested in dropping by.

To deal with this dilemma, plants have evolved several strategies to keep visitors coming and at the same time minimizing pollen loss. Some species hide pollen inside their anthers (poricidal anthers), others produce indigestible or even toxic pollen so that only a few efficient, specialised pollinators can get to it; the palynivore hoi polloi is kept at bay. Another clever approach is to induce bees to be less efficient at grooming, so that more pollen grains are available for deposition on a receptive flower. And one way to accomplish this is through nototribic flowers. This term applies to flowers built in such way that their stamens and style come in contact with the dorsal surface of the bee’s body. They are common in the group of sage, mint and rosemary plants (family Lamiaceae) and figworts (family Scrophulariaceae). 

A honey bee on a meadow clary (Salvia pratensis) flower cut open laterally, and a schematic drawing showing the stamen touching the bee’s back © Reith, M. et al. 2007. Annals of botany 100: 393-400

Bees use their front legs to wipe their heads and antenna, and their middle and hind legs to clean their thoraxes and abdomens (you may have watched a bee grooming itself). But the space between their wings is a blind spot – think about an itch right between your shoulder blades, and you will understand the bee’s problem. The pollen grains deposited in this unreachable area are then taken to another flower.  

Pollen of meadow clary on the back of Bombus terrestris under UV light
© Koch, L. et al.  2017. PLOS ONE 12(9): e0182522. 

Some flowers hide pollen at the bottom of their corollas, and bees such as the fork-tailed flower bee (Anthophora furcata) must creep into these narrow, tubular structures that don’t allow much moving about. The bee vibrates her flight muscles to release the pollen, which gets attached to her head. She pulls out of the flower and scoops up the pollen with her front legs, but not all of it; some grains are stuck to thick, curved hairs between the antennae; these grains can’t be groomed, so become possible pollination agents.

A fork-tailed flower bee has to use her head – literally – to pollinate © Nederlands Soortenregister, Wikipedia Creative Commons

Facial hairs of a fork-tailed flower bee © Muller, A. 1996. Biological Journal of the Linnean Society 57:  235-252

A few plants resort to making life difficult for bees whose habits are not the best for their interests.  And these could be corbiculate bees, that is, bees that carry pollen in their pollen baskets (corbiculae) such as honey bees and bumble bees. Corbiculate bees use regurgitated nectar to stick the pollen together so it can be bundled up nicely for transport. Few pollen grains detach from a corbicula, and the moisture quickly reduces their viability. Most plants live with that, but some would rather save their pollen for bees that transport it on their scopae, which are elongated setae (‘hairs’) on their legs or under the abdomen. These non-corbiculate bees are not as tidy as their corbiculate counterparts: they do not wet and compress the pollen, which is taken away just like dust particles clinging to the hairs of a brush or a broom (scopa, in Latin).

Pollen tightly packed on a bumble bee’s pollen basket (corbicula) (L) and loosely attached to the scopa (fringe of hairs in the abdomen) of a megachilid, a solitary bee © Tony Wills (L) and Vijay Cavale, Wikipedia Creative Commons

To discourage corbiculate bees from making off with their pollen, plants such as the common hollyhock (Alcea rosea) and other mallows (family Malvaceae) produce pollen covered with spines. These echinate (prickly; covered with spines or bristles) pollen grains are relatively large, difficult to handle and to mould into neat pellets. Echinate pollen is a headache for corbiculate bees, the efficient packers, but not a problem for messy pollen harvesters such as solitary bees. As a result, more pollen grains are dropped off from bees, increasing the chances of pollination. 

Echinate pollen grains from three Malvaceae species © Konzmann et al. 2019. Scientific Reports 9: 4705

All these adaptations illustrate the wonderful complexities of an evolutionary give and take: insect pollination is a negotiation between parties with conflicting interests. Plants can’t give away too much pollen but can’t risk being overly stingy: bees would take all the pollen they could handle, but settle for what’s available as long it’s worth their time and energy. Every plant-pollinator combination is an example of a mutually beneficial compromise. It’s natural selection as its best.