The humongous fruit, the tiny pollinator and the duplicitous fungus

By Athayde Tonhasca

Among the range of exotic fruits available to us on grocery stalls, we are not likely to find jackfruit (Artocarpus heterophyllus). But that could change, as the worldwide cultivation and consumption of the fruit have been increasing steadily, fuelled in part by its use as a meat and starch substitute. Jackfruit is a source of dietary fibre and it’s high in potassium and vitamin B. The pulp can be eaten fresh, dried or roasted; seeds can be boiled, roasted or ground into flour. Pulp and seeds can be turned into soups, chips, jams, juices, and ice cream. The jack tree requires little care once it’s been established, and produces high-quality, rot-resistant timber used for furniture and musical instruments. The species is cauliflorous (flowers and fruits grow from trunks and large branches), yielding 150-200 fruits per year. The jackfruit is the largest of all tree-borne fruits, reaching up to 60 cm in length and weighing up to 50 kg. You don’t want to take a nap under a jack tree.

A jack tree loaded with fruit © Crops for the Future, an opened fruit © Kinglaw, and jackfruit seeds and flesh © Aznaturalist. Wikimedia Commons.

Because of all these good points, the jackfruit is frequently cited as a potential contributor to food security throughout the tropics, especially considering the tree’s capacity to withstand high temperatures and droughts. But despite the growing interest in jackfruit, we know little about its reproduction. 

The jack tree is monoecious, that is, it has male and female flowers on separate inflorescences. We are not sure how pollen is transferred between flowers: wind, some beetles and flies have been proposed as possible pollinating agents. Researchers in Florida, USA, found an unexpected candidate: a hitherto unknown species of gall midge (family Cecidomyiidae), Clinodiplosis ultracrepidata (Gardner et al., 2018. International Journal of Plant Sciences 179: 350-367). These midges are attracted by the sweet scent released by the flowers. A midge may get some pollen attached to it when visiting a male flower, and a subsequent visit to a female flower could result in pollination. 

A female C. ultracrepidata and a grain of pollen adhering to the abdomen of a midge © Gardner et al., 2018. International Journal of Plant Sciences 179: 350-367.

But there’s a twist in this relationship: pollination by C. ultracrepidata may depend on the jack tree being sick.    

The fungus Rhizopus artocarpi is a common fungal disease of jackfruit flowers and fruit. It initially infects male flowers, later spreading as a greyish growth of mycelia. The fungus advances slowly until the whole inflorescence or young fruit rot and fall off. Fruit rot, as the disease is known, can cause total loss of fruit if conditions are right for fungus development.

A fruit (A) and a male inflorescence (B) infected with Rhizopus sp. © Ghosh et al., 2015. Biological Control 83: 29-36.

Fruit rot could be bad news if unchecked, but some fungus-covered inflorescences are needed by female midges to lay their eggs and by their larvae to feed and develop. Absence of fungal infestation may break the reproductive cycle of C. ultracrepidata, with unknown consequences for jack tree pollination.

This tale illustrates important facts about pollination. First, we have only the vaguest idea of the players involved; C. ultracrepidata likely originated from Asia, sneaked into America by accident, and remained unknown to science until someone bumped into it. There must be countless other anonymous species quietly pollinating crops and wild plants. Second, we have a partial, often highly speculative understanding of processes. For example, we don’t know how relevant C. ultracrepidata is for the pollination of jack tree flowers in Florida or elsewhere: the study did not rule out other insects or wind as contributors. We also don’t know the equilibrium point in this tripartite relationship, i.e., what’s the level of fungal infestation that’s tolerable for a jack tree and sufficient for midge reproduction.  

There is much to be learned in the field of pollination ecology. Considering its relevance to food security, the economy, and to our health, questions about pollination mechanisms and pollinating agents are worth pursuing.  

Jackfruit for sale in New York City. You may be needing a bigger bag © EdwinAmi, Wikimedia Commons.

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.     

A feathery pollinator

By Athayde Tonhasca

As gardeners across the country gradually come out of hibernation to resume tending their flower pots and vegetable beds, they can count on one visitor for company: the Eurasian blue tit (Cyanistes caeruleus). This little bird is a common sight all year round in gardens across the UK, and it is definitely good company because it spends a good chunk of its time hunting leaf-munching caterpillars – although flies, aphids, beetles, wasps and spiders would also do for lunch. Outside the breeding season, they also eat seeds and buds.

The Eurasian blue tit © Francis Franklin, Wikipedia Creative Commons

This everyday bird and the related great tit (Parus major) came into the spotlight in 1921 when they were found to be behind cases of pilfering from British residences. These birds had learnt to prise open or pierce the foil tops of milk bottles left at people’s doorsteps to get at the layer of cream underneath. And they became really good at it: “The bottles are usually attacked within a few minutes of being left at the door. There are even several reports of parties of tits following the milkman’s cart down the street and removing the tops from bottles in the cart whilst the milkman is delivering milk to the houses.” (Fisher & Hinde 1949, The opening of milk bottles by birds. British Birds 42: 347-357). The technique spread quickly, and by 1947 several places across the UK were recording bottle-opening tits. The birds’ cleverness became a case study in social learning.

Tits having their breakfast © Fisher & Hinde, 1949. British Birds 42: 347-357

The blue tit is also known for its acrobatics: when searching for food, it can cling to walls, hold on to the narrowest twig and hang upside down to explore holes and crevices. The talent for gymnastics offered the blue tit a new opportunity – a boost of energy from flowers of the crown imperial fritillary (Fritillaria imperialis).

This plant from the lily family (Liliaceae) is native to Asia and valued by European and American gardeners for its clusters of bell-shaped flowers. In the UK, these flowers are visited by bumble bees, which are attracted by abundant nectar. Birds may be enticed as well, although most of them have to cut through the top of the flowers to get to the nectar. But not the blue tit: it has the right size and skill to access the flower through its opening, without damaging it.

Crown imperial fritillary or Kaiser’s crown © James Steakley, Wikipedia Creative Commons

Nectar feeding is rare among European birds: in fact, not one species is considered to be a specialised nectarivore. But the blue tit is known for dabbling in nectar now and then from plants like gooseberry (Ribes uva-crispa) and willows (Salix spp.). Different from most passerine birds, blue tits seem to be able to digest sucrose, a quirk that is likely to give them an advantage over great tits, their garden competitors. 

To the crown imperial fritillary, visits by inquisitive blue tits are most welcome. While probing a flower for nectar, the bird touches anthers and stigma, and when it hops to another flower, inevitably pollen is transferred. So, as a first for a plant growing in Europe, the crown imperial fritillary is mainly – or perhaps solely – pollinated by a bird. 

Blue tits visiting crown imperial flowers © Búrquez, 1989. Oikos 55: 335-340

In Europe, 46 or so bird species visit flowers, and it is usually assumed they are looking for insects or other invertebrates. But most of these birds are generalists, feeding on whatever comes to hand. So it’s possible that some of them occasionally go for a sip of nectar, just like the blue tit. And just like the blue tit, a few birds may contribute to pollination. Of the nearly 100 European plants visited by birds, about a third are introduced species like the crown imperial fritillary. If some of them are pollinated by native birds that take advantage of a novel food source, the ecological implications may be profound. We won’t know until the matter is investigated. Who knows, perhaps some bird besides the blue tit will join insects on the list of British pollinators.

Sweet, dangerous attraction

By Athayde Tonhasca

In ancient Greece, nymphs were deities portrayed as gorgeous maidens who would hang around ponds, rivers and other outdoor spots. But their beauty was hazardous: just like those wicked mermaids, nymphs could lure a virtuous man who happened to be passing by, leading him to madness or perdition.

A Nymph abducting the Greek hero Hylas © François Gérard, 1826. Image in the public domain

Nymphs may have been the product of overstimulated male fancy, but they also inspired the name of the water lily plant family, Nymphaeaceae. And just like the Greek nymphs, some water lilies do engage in devious charming, sometimes with fatal outcomes.

© Ann Murray, UF/IFAS Center for Aquatic and Invasive Plants

The white water lily or fragrant water lily (Nymphaea odorata) is an aquatic plant from shallow lakes, ponds, and slow moving waters throughout the Americas. It’s a popular nursery choice for ornamental ponds and water gardens around the world, but its floating leaves can form thick mats of vegetation, sometimes preventing light penetration and retarding water flow. So this plant is considered invasive in some places.

When a white water lily flower opens, its female parts are shaped like a bowl with the stigma (the part that’s receptive to pollen) at the bottom. This bowl is surrounded by a wall of stamens and filled with a viscous liquid full of sugars and detergent-like substances (surfactants). If this rigging has the look of a trap, that’s because it is one. 

© SanctuaryX, Wikipedia Creative Commons

The fragrant flower – hence the epithet odorata – is irresistible to bees, flies and beetles. When a visitor lands, it falls into the bowl. It tries to pull itself out, but the palisade of flexible stamens hinders escape. As the insect struggles, pollen attached to its body is washed off by the liquid. The pollen drifts to the bottom of the bowl where it comes into contact with the receptive stigma, pollinating the flower. The insect may eventually crawl out, or it may drown: it makes no difference to the white water lily. It has got its pollen.

At the end of first day of blooming, the flower closes. When it opens again the next day, it spreads out more widely, no fluid is produced and the stigma is no longer receptive. The stamens release their pollen on the second or third day, and this asynchrony with the female parts prevents self-fertilization. Visiting insects are safe now, so they may fly away covered with pollen – perhaps to meet a watery end on another flower with a receptive stigma. On the fourth day, the flower is pulled underwater, where the seeds mature.

Sweat bees (family Halictidae) are common visitors to white water lilies. Image in the public domain

In South America, giant water lilies (Victoria spp.) take unlawful detention to another level. Their flowers attract and trap beetles until the following day, when they are allowed to leave loaded with pollen. Watch a time-lapse video of a giant water lily flower opening and closing over the course of two days. The flower opens during the receptive stigma phase, closes to entrap beetles, turns pink (pollen release phase), opens again to free its pollinators, then closes before sinking in the water.

By detaining insects for a while, plants increase the probability of fertilization. This type of relationship is known as entrapment pollination, and molecular studies suggest this is one of the oldest pollination systems. Nymphaeales (the order consisting of water lilies and other plants) and beetles have been playing this game for approximately 90 million years. It has worked nicely for both gaolers and gaoled.

Judicious poisoning

By Athayde Tonhasca

Bright lemon-yellow globeflowers (Trollius europaeus) bring a bit of gaiety and colour to damp and shady areas such as woodlands, river banks, upland pastures and meadows across Scotland, northern England and northern Wales. These globe-shaped flowers are unusual: they have tightly-closed sepals that encase the true petals, which have nectaries at their base. They look like big yellow buds at the top of long stems, and rarely open fully. 

Globeflowers © BerndH, Wikipedia Creative Commons

This type of arrangement does not encourage most pollinators because they have hard times getting to the pollen and nectar. But one group of insects doesn’t mind: the root-maggot flies of the genus Chiastocheta, of which five species have been recorded in the UK. These are anthomyids – from the family Anthomyiidae, a name derived from the Greek anthos (flower) and myia (fly). The less flattering ‘root-maggot flies’ comes from the fact that their larvae grow inside stems or roots of various plants.

A fly investigating a globeflower © Uoaei1, Wikipedia Creative Commons

Male and female flies wiggle their way towards the flower’s nectaries. Once inside, they feed and mate, pollinating the flower in the process. Male and female are hairy, so pollen gets attached all over their bodies. But females need more than food: as true root-maggot flies, they deposit their egg on the carpels (the flower’s seed-bearing structures), and the resulting larvae develop and feed on the seeds. So Chiastocheta spp. are simultaneously pollinators and seed predators.

A female Chiastocheta setifera © Janet Graham, Wikipedia Creative Commons

Insect pollination is a mutualistic relationship, where each partner benefits from the other: the pollinator gets food or some other reward, while the plant gets fertilized. Another way of seeing it is as reciprocal exploitation: flowers produce as little pollen and nectar as necessary to attract pollinators, and insects would take away as much of those resources as flowers allow. So flowers must maintain a fine equilibrium between attractiveness and the metabolic costs of producing pollen and nectar. In the case of globeflowers, there is the added burden of seeds lost to root-maggot flies.

Seed head of a globeflower: cosy growth chambers for root-maggot flies © Ivar Leidus, Wikipedia Creative Commons

To avoid over-exploitation by Chiastocheta spp., globeflowers resort to chemical defence. Like other species of the buttercup family (Ranunculaceae), globeflowers are slightly poisonous: they produce compounds that discourage plant feeders. One of these chemicals, adonivernith, plays a regulatory role in the pollination/seed parasitism balance. Adonivernith is spread all over the plant, but concentrates in the flowers (it contributes to their bright yellow coloration). If the number of larvae growing inside the flower increases, the amount of adonivernith also increases, eventually inhibiting larval growth and feeding. It’s the globeflower’s way to regulate the loss of valuable seeds for the sake of pollination: when flies become a liability, they are curtailed by intoxication.  

Male flies are also important for maintaining the right balance between pollination and seed predation. They are smaller and transport less pollen than females, but make about twice as many flower visits during the same time period. Male pollination incurs no seed losses, so they help reduce the pressure on their host. 

In nature, it’s often a matter of harmonizing antagonistic interests.   

Fig wasps, evolutionary marvels

By Athayde Tonhasca

When people talk about keystone and indicator species, often what they mean is ‘my favourite species’, or ‘the important species I work with’. But one group of organisms truly deserves the label of keystone species: figs. The genus Ficus comprises over 900 species spread throughout the tropical and subtropical regions as shrubs, lianas (woody vines), or trees. Strangler trees – which don’t strangle anything – are one of the best known types of fig plants.

Many fig species produce fruit asynchronously throughout the year, so many animals have a steady supply of abundant and nutritious food. This is especially important during the dry season, when most plants do not fruit. Figs are often preferred even when other fruits are available because they are rich in calcium, a mineral usually in short supply. So figs are essential for a wide range of birds and mammals such as pigeons, toucans, parrots, macaws, bats, peccaries and monkeys. Over 1,200 vertebrate species feed on figs.

The strangler fig Ficus aurea © Forest Starr and Kim Starr, Wikipedia Creative Commons, and the diversity of fig characteristics © Lomáscolo et al. 2010. PNAS 107(33):14668-72

Figs support the diversity and functioning of ecosystems around the world, but they can only do that thanks to some tiny wasps.

Chalcid wasps are an enormous group of insects, estimated to contain over 500,000 species. Most of them are parasitoids of other insects, but a small group belonging to the family Agaonidae has one purpose in life: to get into a fig to reproduce. By engaging in fruit breaking and entering, these wasps, appropriately known as fig wasps, pollinate the fig plant. 

A female fig wasp © Robertawasp, Wikipedia Creative Commons

The mission is made immensely complicated by figs’ morphology. Botanically speaking, a fig is not a fruit but a type of inflorescence known as a syconium (from the Ancient Greek sykon, meaning ‘fig’, which originated ‘sycophant’, or ‘someone who shows a fig’; a term of curious etymology). A syconium is a fleshy, hollow receptacle containing simplified flowers or florets, and each floret will produce a fruit with seeds in it. A fig harbours dozens to thousands of florets and fruits, depending of the species. The crunchy bits of the fig we eat are not seeds but fruits.

Florets need pollination, not an easy proposition when they are bunched up and locked inside a container. So the fig wasp’s first hurdle is to get inside the fig. A female wasp does it through a hole at the bottom of the fig (the ostiole), which loosens when the fig is ready for pollination. 

Longitudinal section of a syconium. The inner wall of the hollow chamber is covered with florets, and the ostiole at the bottom is the door for female wasps © Gubin Olexander, Wikipedia Creative Commons

A receptive fig does not make life much easier for the female wasp. She has to chew her way through, pushing and squeezing, often having her wings and antennae snapped off in the process. She will find a floret, insert her long ovipositor into it and lay an egg. As she’s busy doing that, pollen grains attached to her body get rubbed off onto nearby florets, assuring their pollination. With the job done, the female wasp dies.

The ovules of florets that receive eggs will form galls in which the wasp larvae develop, while pollinated ovules turn into fruit. The adults chew their way out of the galls, males first. Sometimes they help females get out from their own florets and mate with them. Males will then chew a hole through the fig wall to let the females escape. Males stay behind: they couldn’t go anywhere, as they have no eyes and no wings. After an ephemeral life spent entirely inside a fig and marked by moments of glory such as fertilising females and setting them free, males die. 

A male (L) and a female fig wasp recently emerged from their galls. The male is using his mandibles to open a gall containing a female to let her escape and be the first to mate with her © van Noort et al. 2013. African Invertebrates 54(2): 381-400

A female collects pollen grains from intact florets or picks them up by accident before braving the world outside. She will follow the trail of chemicals released by a host plant to find another fig receptive to pollination and start the cycle again. But she must be quick: she has a few hours to three days to live, depending on the species. And to complicate things, not any fig will do. Each species of fig tree is pollinated by one or a few host-specific fig wasps, which is an outstanding case of coevolution. 

The great majority of female wasps don’t make it, but a few do: they catch rides on wind currents above the canopy to find host plants over 10 km away, farther than most pollinators. This is a remarkable achievement for such small, fragile, and short-lived insects. 

You can learn much more about figs and fig wasps at Figweb from Iziko Museums of South Africa.

Perhaps nothing exemplifies better the wonders of fig pollination than the exploits of Ceratosolen arabicus in Namibia. This wasp pollinates the African fig tree (Ficus sycomorus) along the Ugab river in the North Namib desert. This is one of the most inhospitable and remote corners of the planet, famous for its Skeleton Coast, a place of shipwrecks and marooned sailors. African fig trees occur in isolated clumps along the riverbank, but that’s not a barrier for the wasp: it covers average distances of near 90 km and a maximum of 160 km over the desert at night in search of a receptive fig. As the wasp survives for 48 h or less, this quest must be quick and efficient.

Dry Ugab riverbed, Namibia © Theseus, Wikipedia Creative Commons

How do figs and fig wasps relate to us, denizens of fig-less countries? This pollination system has a profound influence on global biodiversity and ecosystem functioning, so it affects us as well, even if indirectly. The story of figs and wasps also illustrates the capabilities, drive and hardiness of minute, easily overlooked insects that are so important for us and nature.

Pollination: a wealth and health trade

By Athayde Tonhasca

For centuries, berries of the açaí palm (Euterpe oleracea) have been a staple food for the people in the Amazon, thanks to the fruits’ high caloric content. In the 1990s, açaí (ah-sah-ee), served as frozen pulp or juice, became a fashionable street food in Brazilian cities, a craze boosted by bogus claims about ‘antioxidant’ and ‘superfood’ properties. In no time the purplish berry left its swampy Amazonian plains to conquer the world: today açaí na tigela (açaí on a bowl) is available in restaurants and health food joints across Europe, America and Japan. 

Açaí berries and a traditional bowl of açaí with fruit and granola © CostaPPPR (L) and Gervásio Baptista, Wikipedia Creative Commons

Açaí generates an estimated US$ 1 billion/yr for the Brazilian economy, and the market is growing at a brisk pace. Most berries are harvested from palms growing in the wild, and everyone enjoying their benefits – subsistence farmers, traders, exotic food buffs and the taxman – must be grateful to the insects that pollinate the palm’s inflorescences, mostly stingless bees.

Stingless bees Trigona pallens, big contributors to the Brazilian economy © Nemésio, A. et al. 2013. Brazilian Journal of Biology 73: 677-678

The açaí berry is just one of several pollination-dependent products exported from Brazil and many other countries. When all the data is put together, it is estimated that more than 50% of the world’s exported crop products depend on pollinators.

Log-transformed tons of exported pollination-dependent Brazilian crops, 2001–2015 © Silva et al., 2021. Science Advances 7, eabe6636

Deforestation, fires and habitat degradation – which includes the spread of crop monocultures – threaten this global pollination-based trade, with heftier consequences for developing countries.  We may shrug our collective shoulders at what seems to be other people’s problems, but we must remember that a significant portion of the vitamins and minerals essential for our diet comes from insect-pollinated food, and most of it is imported. Many types of apples, pears, avocados, citrus fruits (e.g., orange, tangerine, limes, grapefruit) cucurbits (such as melon, courgette, cucumber, squash), peas and beans benefit from or are greatly dependent on insect pollinators, although some varieties are self-fertile and need none. Most vegetables consumed in the UK don’t require pollination for yield, but many of them may need pollinators for seed production; these include brassicas (broccoli, Brussel sprouts, cauliflower, cabbage, kale, etc.), carrot, fennel and parsley.

Pollination is important for our nutritional needs, and also for a few of our pleasures and indulgences. We may carry on through life without a bowl of açaí, but much less happily in the absence of coffee or cacao (hence chocolate), both of which need pollinators for adequate yield and high crop quality. House parties are more satisfying when stocked with bowls of almonds, Brazil nuts and cashews, none of which would be available without insect pollinators. If it wasn’t for bees, Worcestershire sauce wouldn’t be on the dinner table, at least not in its existing version. The condiment contains tamarind extract, and the tamarind tree needs bees for pollination. The list of examples can be quite long.

No nuts or Worcestershire sauce without pollinators © Melchoir (L) and Bardbom, Wikipedia Creative Commons

Brexit and the Covid pandemic have sharpened our attention to food security, so perhaps pollination, which is important to our diet, health, wellbeing and economy, will get a brighter spotlight. But just like climate change, threats to this ecological service are not confined by borders. Deforestation, pollution, wildfires and biodiversity losses may hurt far-flung places first, but their effects will cascade down to us. More than ever, we need to ‘think globally, act globally’.

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.

Einstein’s bees, sound bites and vitamins

By Athayde Tonhasca

If you have been following the news about bees’ decline in the newspapers and social media, you’ve probably come across variations of this quote, attributed to Albert Einstein: “If the bee disappears from the surface of the earth, man would have no more than four years to live.” This insight from one of the greatest scientist who ever lived seems to corroborate another mantra: “one in every three bites of food we eat depends on bees”. So the message from these sound bites is clear and dire: bees’ extinction would lead to food shortages, widespread famine, and ultimately the extinction of mankind.

Considering the seriousness of the matter, we may feel a bit disappointed by Einstein’s vagueness: did he mean the honey bee alone as humanity’s saviour, or the other 20,000 or so known species as well? But don’t blame Einstein for this taxonomical oversight because the quote is a myth: he never said it. Which is not surprising, really; would it be reasonable to expect the man who revolutionized our understanding of space, time, gravity and the universe, to have the time and knowledge to lecture us about bees as well? Probably not. Could the eminent evolutionary biologist Richard Dawkins offer new insights about the Special Theory of Relativity? Probably not. Authority has boundaries, and experts generally know their limitations.

Einstein’s prophecy belongs to the extensive list of fake quotes attributed to him and the likes of Abraham Lincoln, Mark Twain and Winston Churchill. But at least we know that one of every three bites of food we eat depends on bees. Or do we?

The 1 to 3 ratio could be read as the amount of food we eat by weight or by volume, or the proportion of food items in our diet. The latter is the usual interpretation of the quote, which originated from a misinterpretation of a 1976 report by the American Department of Agriculture.

But here are the data. Nearly 90% of the world’s caloric intake comes from rice, maize, millet, barley, sweet potatoes, bananas, wheat, sorghum, rye, potatoes, cassava and coconut. Only the last crop may require some insect pollination. About 60% of global food production comes from crops that do not depend on animal pollination: they are wind-pollinated, self-pollinated or propagated asexually. 

But how about the number of food items? Around three-quarters of the world’s main crops benefit from animal pollination (insects, birds, bats, etc.). But ‘benefit from’ is a far cry from ‘depend on’; pollination is not an all-or-nothing scenario. Crops have diverse degrees of reliance on pollination (see figure), which does not necessarily reflect on yield, but sometimes on product quality or shelf life. Only about 12% of the main crops depend entirely on pollinators to produce the food we consume.

Level of dependence on animal pollination of the main crops produced in 200 countries. Data from Klein et al. 2007. Proc. R. Soc. B 274: 303-313

The ‘1 in 3’ formula ignores meat in our diet. It’s difficult to evaluate the contribution of pollination to meat production considering the range of animal species and production systems. But it is safe to say that the bulk of animal protein originates from plants that don’t need animal pollinators such as grass, maize, and soybean. 

The proportion of animal-pollinated food of course depends on cultural backgrounds, dietary preferences and economic status, but it is not likely to be that great. You can check it for yourself: make a list of non-meat items on your dinner plate and look it up as to whether they are pollination-dependent (you may exclude the pizza and fish & chips dinners).

None of the above undermines the importance of pollination. This ecological service is estimated to account for around 10% of the world’s annual agricultural output; we could expect losses of 5 to 8% in total crop production in the absence of animal pollination. In the EU, 15% of crop production involves pollination, which generates around 31% of the income from crops. These figures are far from inconsequential. And the importance of pollination stretches way beyond yields and income: nearly 90% of the world’s flowering plants require animal pollination, so the whole functioning of the planet is linked to pollinators.

Like any good sound bite, “one in three bites” is memorable and catchy; but as it is often the case with sound bites, it is unclear, inaccurate and simplistic. It also distracts us from pollination’s real contribution to food production, which is the quality of our diet.

Most of the vitamins A, C, and E we need come from animal-pollinated plants such as vegetables, nuts, seeds, and fruits. The same is true for a large portion of vital minerals such as calcium, fluoride and iron. A decline in pollination services would decrease the supplies of these crops, which inevitably would result in higher incidence of diet-related illnesses such as heart diseases, cancer and diabetes. Fewer animal-pollinated fruits and vegetables in our diet would also contribute to the ‘hidden hunger’, which is a form of malnutrition caused by a lack of vitamins and minerals in the diet. Close to 2 billion people worldwide suffer from ‘hidden hunger’; this figure could be brought down by the addition of minerals and vitamins to staple foods, and by protecting pollinators that provide this public health service for free.

The proportion of food production that is dependent on pollination for vitamin A (a) and iron (b) © Chaplin-Kramer et al. 2014. Proc. R. Soc. B 281: 20141799

Pollinators do not contribute significantly to our caloric necessities; the number of bites of food that depend on bees is relatively small. But these few bites are essential for our nutrition and consequently to our health. In a country where 1 in every 4 adults and 1 in every 5 children are estimated to be obese mostly because of poor diet and lack of exercise, reducing the number of bites we eat should be a national priority. But improving the quality of those bites is equally important, with more fruit, vegetables and nuts on our plates: here’s where pollinators make their greatest contribution to our wellbeing.

May the Force be with the bee

By Athayde Tonhasca

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 is just beginning to be understood: electricity.

It has long been known that the platypus, some fish and amphibians, as well as some ants, cockroaches, mosquitoes and fruit flies have the ability to detect external electric forces. However, 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. 

We do not notice it, but our planet is an immense electrical circuit. On a calm day, the air is positively charged, while the ground surface has a negative charge. Now and then the equilibrium of charges is disturbed by lightning bolts or a minor shock from a car door, reminding us we are surrounded by electricity.

The negative charges accumulated on the planet’s surface extend to any object connected to the ground, plants included. So flowers have a slight negative charge in relation to the air around them. As a bee buzzes along in search of food, electrons are stripped off its body by friction with the air, leaving the bee positively charged. When the bee lands on a flower, some of the negatively charged pollen grains stick to the bee, sometimes jumping from the flower even before the bee makes contact. So electrostatic forces are a great aid to pollination.

An electrifying encounter: a positively charged bee approaches a negatively charged flower. Images in the public domain.

Pollen clinging to a sweat bee. © Pixabay.

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 rubbed 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 is as if the bee ‘sees’ the flower’s electrical aura. 

Bumble bees’ 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 remains changed 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 charges 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 radically differently from ours.