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.

Smorgasbord or Spartan: the consequences of pollen diets

By Athayde Tonhasca

There is nothing visibly remarkable about the mining bee Andrena florea. This bee, one of the 67 Andrena species in Britain, is found in open scrubby areas, grassland and woodland edges of south-east England. But one thing makes this bee unusual; it only takes pollen from white bryony (Bryonia dioica).

Andrena florea, which is commonly and unsurprisingly called the white bryony mining bee, is a rare British example of a bee that forages on a single plant species. This dietary restriction is circumstantial, because white bryony is the only plant of this group occurring in Britain. In continental Europe, A. florea has other Bryonia species available. So in a wider geographical context, this bee is oligolectic (or an oligolege) that is, it collects pollen from a few related plant species (from the Greek oligo: few, scant; and lect: chosen, picked).

A white bryony mining bee and its pollen source, white bryony © Aiwok (L) and H. Zell (R), Wikipedia Creative Commons

Pollen specialisation can be a considerable drawback for a bee because food may be scarce even in a landscape full of flowers, and this may limit populations of some species. For example, until recently the white bryony mining bee was rare and threatened in Poland. This has changed with the spread of white bryony into the country’s urban areas. And yet, a considerable number of species are pollen specialists; in some habitats, they make up the majority of the bee fauna. So pollen specialisation must have its advantages, for example by allowing more efficient flower visitation and pollination rates, which benefits bees and plants.

Polylectic bees are at the other end of the spectrum: they collect pollen from various unrelated kinds of flowers. The advantages of being a pollen generalist seem evident: there is more food to choose from and it’s available for longer, as flowers blossom at different times. But these bees must also have an array of physiological adaptations to overcome a variety of chemical and physical barriers to different types of pollen. This could be too costly for a bee’s metabolism.

Pollen is a rich source of protein, lipids, vitamins and minerals. But it also contains secondary compounds that may be noxious to some bees, and pollen grains are often protected by indigestible coating. These barriers explain why few insect taxa rely on pollen alone for food, and could also explain why most polyleges (polylectic bees) exhibit a degree of pollen specialisation: for example, heather (family Ericaceae) and legumes (family Fabaceae) make up over 70% of the pollen collected by British bumble bees, despite local abundance of other pollen sources.

Experiments with the closely related red mason bee (Osmia bicornis) and horned mason bee (Osmia cornuta) show the effects of different types of pollen. Red mason bee larvae develop well on buttercup pollen (genus Ranunculus), but fail to do so on pollen from viper’s bugloss and related plants (genus Echium); the reverse happens for the horned mason bee. Both bees do well on field mustard pollen (genus Sinapis), while neither develop on pollen from tansies and related species (genus Tanacetum). But the story is a bit more complex: neither bee shows any negative effect as long as they are not restricted to ‘bad’ pollen. In fact, unsuitable pollen is part of the bees’ natural diet. Other bee species show similar patterns.

Viper’s bugloss (1), creeping buttercup (2), field mustard (3) and tansy (4): nutritious/poisonous food for the right/wrong bee. © Wikipedia Creative Commons

So what can we conclude from all this?

Oligolecty and polylecty are both successful evolutionary strategies. Some bees depend on a few plants, others have diversified pollen diets. The range of hosts can be narrow or wide, depending on the species, but setting aside a handful of exceptions, bees need pollen from different plants to complement nutritional imbalances or to mitigate the effects of harmful secondary metabolites. But even pollen of low nutritional quality or digestibility is taken, as long as it’s a portion of a balanced diet.

These aspects have important consequences for the conservation of bees. They need a diversity of flowers, and plenty of them. Habitats such as semi-natural grassland, hedgerows, field borders, cover crops, brown sites, road verges, wild gardens and weedy parks are all suitable. Planting is helpful, but except for the honey bee and some bumble bees, we know little about what plant species to use. The safest action is to let our wild plants go wild, so that we have bigger, and more diverse flower-rich habitats. That’s not much or too difficult a task to assure the future of our most important pollinators.  

A healthy diet for fussy eaters

By Athayde Tonhasca

Pollen, the fertilizing agent that carries the male gametes (reproductive cells) of flowering plants and grasses, is packed with protein, starch, sugars, fats, vitamins, and inorganic salts: carotenoids and flavonoids add the colouring. This rich resource wouldn’t go untapped by many insects and mites. Among them, bees are the ultimate palynivores (pollen eaters).

To us humans, one pollen grain is indistinguishable from the next: it’s that granular yellow stuff that may cause seasonal allergies such as hay fever. But pollen of different plant species comprises a smorgasbord of chemicals. Protein, by far the most important nutrient as the source of vital amino acids, ranges from 2 to 60% of pollen dry mass. The composition and amount of other essential nutrients vary as well. Some pollen contains secondary metabolites such as alkaloids and glycosides, which are harmful to some bees: buttercups and related species (Ranunculus spp.) for example are toxic to honey bees. Pollen grains of some plant families are coated with a sticky substance called pollenkitt, which probably helps pollination. But just as some people can’t digest lactose, some bees can’t digest pollenkitt.

Miscellaneous pollen grains © Dartmouth College Electron Microscope Facility, Wikipedia Creative Commons

Bees have adapted to the range of pollen quality by adopting diversified diets: most species are polylectic, that is, they collect pollen from various unrelated plants (as opposed to oligolectic species, which specialize on a few related plants). By taking pollen from many sources, bees get a balanced diet and reduce the relative intake of harmful chemicals. When polylectic bees are fed pollen from a single source, they often fail to reproduce or die. The need for nutritional diversity has deep implications for bee conservation. 

Agri-environment programmes throughout Europe have promoted the creation of flower-rich habitats to reduce the impact of agriculture intensification on pollinators. Field margins and other non-crop areas are planted with seed mixtures, and the practice has made a difference: bumble bee declines have slowed or sometimes reversed in recent decades. As a bonus, honey bees and butterflies have benefited as well. However, most solitary bees (which make up about 90% of the approximately 250 species of bees in UK) have been unintentionally left out.

Two of our solitary bees: a miner bee © Pauline Smith, and a leafcutter bee © Saxifraga – Pieter van Breugel

It turns out that seed mixtures comprise a high proportion of legumes (family Fabaceae) such as red clover, white clover and vetch. These plants are good for bumble bees, but are not the best or not suitable at all for many solitary bees. Most species get their pollen from plants such as smooth hawk’s-beard (Crepis capillaris)scentless mayweed(Tripleurospermum inodorum), field bindweed (Convolvulus arvensis), rough chervil (Chaerophyllum temulum), meadow crane’s-bill (Geranium pratense) and dandelions (Taraxacum agg.). Species from the families Asteraceae (daisies, marigold, snakeroot, tansy, thistles) and Apiaceae (cow parsley, wild carrot, ground elder) are also important. 

Weeds or food for pollinators? Smooth hawk’s-beard (L) © Michael Becker, Wikipedia Creative Commons, and wild mustard (R) © Hectonichus, Wikipedia Creative Commons.

These plants grow naturally in and around arable fields, but some of them are not welcomed by farmers because of their invasiveness. Wild mustard (Sinapsis arvensis) and wild rose (Rosa canina) for example are excellent sources of pollen for solitary bees, but the first is a serious weed of oilseed rape fields and other crops, and the latter is a climbing shrub, not suitable for field margin management. 

The inclusion of weeds in seed mixtures may not be an option, but a more tolerant attitude towards them would be beneficial and safe. A wild plant does not become a weed until it starts competing with crops, and this threshold may take a while – or it may never be reached. The same principle applies to our gardens: we don’t need to kill weeds willy-nilly for questionable aesthetic reasons.

As in so many areas of conservation, the answer lies in finding a middle ground. We need to cultivate an appreciation for wildness over manicured fields and gardens because just as a varied diet is best for human health, a diversified flora represents an essential buffet for bees and other pollinators.