Three’s a crowd

By Athayde Tonhasca

The Brazilian north-eastern hinterland is not a hospitable place for an outsider. Except for a short and intense rainy season, this is a dry, dusty and sizzling territory: a land of the cactus, thorny scrub and stunted trees. The native Tupi speakers called this semiarid region caa (forest, vegetation) tinga (white), and the term was adopted by the Portuguese settlers as caatinga. But the apparent harshness of the landscape misrepresents its ecological importance. The caatinga is a biota found nowhere else in the world, harbouring more than 2,000 species of vascular plants and vertebrates, with endemism in these groups ranging from 7 to 60%. And like every other Brazilian ecoregion, the caatinga has been severely degraded and fragmented.

The caatinga landscape © Maria Hsu, Wikimedia Commons.

Rain in the caatinga is unpredictable, even during the rainy season: there could be flooding downpours, scattered drizzles, or no precipitation at all. This erratic pattern doesn’t seem to be the safest for aquatic plants, which have to make do with seasonal water courses and ponds that persist from weeks to a few months at best. But this ephemeral habitat is not a problem for the water poppy Hydrocleys martii, (family Limnocharitaceae), which is common in the caatinga.

The water poppy H. martii © Yikrazuul, Wikimedia Commons.

Relying on short-lived, unreliable water bodies is tricky for an aquatic plant, but the water poppy has another particularity that pushes its luck in the survival game: it seems to be pollinated by a single flower visitor, Protodiscelis palpalis, a plasterer bee (family Colletidae). Even more remarkable, this bee is a monolectic species, that is, it collects pollen from a single host plant. In other words, plant and bee are entirely dependent on each other. 

Such restricted association requires careful fine-tuning, which plant and insect accomplish with flying colours.

Blooming is a hurried affair for the water poppy. Its flowers develop underwater, and emerge on the tips of pedicels when mature. They open on the following morning and close again in the early afternoon; the pedicels then curve downwards and the flowers disappear under water, where fruits will develop. During the four hours or so that a flower is open for business, many bee species pay a visit. But most of them can’t get to the pollen because the flower’s anthers and stigma (their reproductive organs) are hidden behind a wall of staminodes – these are sterile stamens found in some plants that prevent self-pollination. But this morphological barrier is not a problem for P. palpalis bees: they use their heads and forelegs to push through the staminodes and reach the pollen in the centre of the flower. And these bees don’t faff about: within one hour of blooming, they gather about 80% of the ~480,000 pollen grains produced (Carvalho & Schlindwein, 2011).

A flower bud at the end of a pedicel, and an open flower with its reproductive organs surrounded by staminodes © L.Q. Matias, Reflora.

Bees are quick at collecting pollen and also at finding it. They locate a receptive flower through a combination of visual and chemical cues: its bright yellow colour and a cocktail of 22 scent compounds (Carvalho et al., 2014). This skill is no small matter in a hostile environment where plant populations may be kilometres apart. 

A male P. palpalis stays put on a H. martii flower © Airton Torres Carvalho, Grupo ASA.

Monolecty is not confined to exotic, faraway places. In the Iberian Peninsula, only the pollen from Cistus crispus(family Cistaceae) will do for the mining bee Flavipanurgus venustus (family Andrenidae). And just like in the caatinga case, these two species have developed a close bond: periods of bee flying and plant blooming are synchronized, and bee numbers are correlated with host plant numbers (González-Varo et al., 2016).

c, d: females F. venustus with their scopa loaded with C. crispus pollen; e: a male in the top-left corner approaches a female in its territory © González-Varo et al., 2016.

The false alkanet (Anchusa barrelieri, family Boraginaceae) and the endangered plasterer bee Colletes wolfi are another example of close plant-pollinator association. This plant, a European native, does not make life easy for pollen collectors: its anthers are hidden behind scales inside a narrow tube. But on the Italian peninsula, C. wolfi is equipped to deal with the challenge. Its legs are short – when compared to other European plasterer bees – and armed with sturdy, curved bristles, which are perfect for scraping off pollen from flowers. And C. wolfi has to do the job well, as the false alkanet is its only host (Müller & Kuhlmann, 2003).

A false alkanet flower © Frank Coulier, Observation.org.

Foreleg (L) (bar = 500 µm) and tarsus (bar = 300 µm) of a C. wolfi female © Müller & Kuhlmann, 2003.

The white bryony mining bee (Andrena florea) and the ivy bee (Colletes hederae) are oligolectic, that is, they collect pollen from a few plants, typically from the same genus or related genera. But here in Britain, they are functionally monolectic because each bee has a single host plant.

These pollen specialists face significant shortcomings because their food may be scarce or absent even in a landscape chock-full with flowers. But since many bee species do specialise to some degree, there must be selective advantages for being picky. Specialists may compensate for their narrow diet by gathering more pollen and faster than polylectic species (those that collect pollen from many unrelated flower species); they may have become adapted to plants’ chemical defences, thus getting resources not available to their rivals; or they may suffer less from the effects of direct competition with other flower visitors (Danforth et al., 2019).

For a bee, being a pollen specialist is no better or worse than being a generalist: both are successful evolutionary strategies that have worked for individual species. But this array of feeding habits has practical consequences: to protect the bee fauna – and other pollinators for that matter – we need to provide them with the right type of flower. To increase the chances of doing it right, we have to conserve and create diversified, flower-rich habitats, so that even the pickiest flower visitor is likely to find the food it needs.

Dundee’s positive changes

They’ve been busy in Dundee.  Very busy.  Dundee City Council has been implementing a range of measures to help biodiversity, and, as part of a review of grassland management, the Council held a public consultation on changes to 27 parks and greenspaces. The aim has been primarily nature-friendly management. 

Newly seeded biodiversity grassland at Dawson Park in Broughty Ferry

Dundee currently boasts 49.5 ha of natural grasslands, with a further 10 ha described as biodiversity grassland. Those naturalised grasslands are cut once a year but the cuttings aren’t lifted, whereas in the biodiversity grasslands areas one or two cut are carried out each year and the cuttings are lifted. These areas already had a good range of common wildflowers

Some of the latter areas have been additionally sown with yellow rattle (aka the meadow maker) whilst others have had perennial wildflower seeds introduced to improve the sites and hopefully reduce the amount of intervention needed in future. In addition, Nature Restoration Funding allowed for the purchase of new machinery to assist in the ‘cut and lift’ management of these areas. This will reduce nutrient levels and help the wildflowers gain a foothold.

The creation of a new perennial wildflower meadow created at the city’s Scott Street was made so much easier by working hand-in-hand with the Friends of Balgay community group. Situated in the west end of Dundee, the area has several wide-open green spaces, as well as secluded areas with seating. The Friends group have been active for several years, promoting the Balgay Park and working closely with the Council to make space for nature.

At the other end of the financial spectrum, the ‘Broughty Ferry to Monifieth Active Travel project, funded by Transport Scotland through Sustains ‘Scotland’s Places for Everyone’, includes the creation of significant areas of native coastal grassland. Works along the Esplanade have seen the removal of non-native shrubs, dunes planted with Marram and sea lyme grasses, and what should in time be an impressive avenue of trees. To complete the activity, three hectares of coastal grassland seeding took place during Autumn 2023. 

About one hectare of annual wildflower areas was sown and managed in 2022, and the council aimed for a similar area to be created in 2023. An additional three hectares of wildflowers were sown in partnership with the Eden Project at Morgan Academy, Riverside Drive and Camperdown Park, with striking interpretation providing highlighting the importance of these areas to pollinators.

Newly seeded biodiversity grassland at Magdalen Green in the West End

Anyone concerned by the threats facing pollinators will have a keen interest in insecticide and herbicide use. Dundee City Council is reviewing herbicide policies with the aim to reduce overall use and to explore alternatives. Mechanical weed rippers were purchased for use on hard surfaces, and additional street sweeping carried out in 2022 to remove the detritus that builds up allowing weeds to colonise. Overall, the volume of herbicide used by Dundee City Council has reduced by 66% in the last 5 years, with a reduction of 45% since the publication of the city’s Biodiversity Action Plan in 2020. 

Ornamental flower and shrub beds have also fallen under the Council spotlight. 

At Seabraes, on the Perth Road, revamped flower beds were revised and pollinator-friendly plant species, provided a haven for invertebrates. Other project areas included Baxter Park, Balgay-Blackness Road seating area, Lily Walker Homeless Unit and Camperdown Park. The projects in these sites focus on tree planting, creation of perennial wildflower areas and wildlife-friendly bulb and herbaceous perennial planting to deliver biodiversity benefits.  

And, in a departure from the bigger park projects, two new ‘pocket parks’ were created at Lorimer Street and Moncur Crescent. The planting within these mini-parks includes trees and herbaceous perennials and grasses, thus bringing valuable new habitats in very urban areas.

The Council obtained an additional £262,000 from the Scottish Government’s Nature Restoration Fund for the creation of Climate Resilient Woodlands. Twelve hectares were planted with 28,000 native trees at Riverside Nature Park, Balgay Hill and an area next to Clatto Country Park. Amongst the trees are wild cherry, crab apple, hawthorn and blackthorn all of which are particularly good for a range of pollinator species.

Of course, what strikes one party as good works, may perplex or annoy another, hence changes sometimes need to be explained. In a Facebook post Dundee City Council alerted residents to the changes. They acknowledged that some residents might see change in the city’s green spaces and “wonder why small areas of local parks aren’t being mowed like they used to be?”

Biodiversity grassland area at Myrekirk Park in the West End, seeded with yellow rattle

The answer, the council explained, is that “In Dundee we are creating carefully managed biodiversity havens. Greater levels of biodiversity helps to ensure the natural sustainability of all life, which is especially important in a time of global climate change.”  Communicating the purpose of change is an oft undervalued, but essential, step if changes are to gain traction and support locally.

What is happening in Dundee is undoubtedly good for pollinators. It fits well with the European environmental zeitgeist. The forthcoming EU Nature Restoration Law includes targets to reverse the decline in pollinators and to restore degraded ecosystems. 

And Dundee is nothing if not innovative. In 2014 the city was named the UK’s first UNESCO City of Design. That title recognised diverse contributions to fields including medical research, comics, video games and Dundee is of course now home to the superb V&A Dundee: Scotland’s first design museum. Now it seems the designs the city has for biodiversity, and pollinators, are drawing equally admiring glances.

Iona’s divine inspiration

Teresa Hughes is our guest blogger today.  An Ecologist and Environmental Advisor with Historic Environment Scotland (HES), she brings us up to date with successful nature-friendly steps being taken around one of Scotland’s most famous historic and spiritual sites, Iona Abbey.

© Historic Environment Scotland.

All the staff at Iona Abbey have recently embarked on a bit of a ‘grassland revolution’. Visually, as well as ecologically, this has had a beneficial impact. We’ve adopted three different types of mowing across our site and are noting considerable ecosystem benefits from the changing habitat structure.

“What are the new approaches?”, I hear you ask. 

We have long-grass areas that will only receive one annual cut. That cut doesn’t take place until mid-August at the earliest as this will allow for a lengthy flowering period and for seeds to set. We also cut this from the centre outwards to allow small mammals and sheltering birds and insects ample escape routes. These areas provide a valuable source of food for pollinators and ground cover for small mammals. 

White clover is benefitting from the relaxed mowing regimes

Our medium areas are maintained at a 150 to 200mm sward height.  Cut more frequently than our long grass areas the medium area nevertheless has low growing flower species such as clovers and bird’s-foot trefoil. These provide a fantastic resource for pollinators, and  the cuttings will be removed to keep nutrient levels in check helping the flowering plants to flourish. This level of sward and more regular cutting will simultaneously ensure the underlying archaeology and interesting ground features remain easy for visitors to appreciate and see.

Finally, our short cut grass areas. Here the aim is to ensure that the Abbey itself is framed, and simultaneously visitors can see that the surrounding grounds are actively managed. 

One of the most obvious outcomes of our change in mowing approaches is a pleasing increase in the diversity of flowering plants. That’s good news for pollinators, of course, but it’s clear that the longer grassland is providing substantive benefits for other species. I am confident that year-on-year we will see increases in floristic diversity too.

Longer grasses provide cover for moths, butterflies and a range of other insects. The longer length of grass protects against rain to some extent, provides shelter against wind, and is a slightly warmer place. This is particularly important when the weather is changeable and showery. 

That showery weather can create interesting insect encounters. Visitors, of which there are thousands,  might notice that after rain, when walking through the longer grass, more insects are ‘put up’ as they have been sheltering near the bottom of the grass. 

The meadow brown butterfly is one species enjoying the new management practices

Several species of butterfly, like the meadow brown, use grasses to lay their eggs on, and likewise many other caterpillars’ and moth’s food plants are grasses. 

The orange tip butterfly is also found on Iona, and feeds on the early flowering lady’s smock. In addition the species has been using the longer grass cover for its overwintering stages.

Iona Abbey, sedum on the rock allowed to flower

The white clover that was already present, provides plentiful nectar for bumblebees. Those species with tongues long enough to reach into the nectary at the bottom of each of the many little flowers that make up the head of the clover flower are set to benefit.

It isn’t only insects that are reaping rewards from the new approach. Grasses and other plants, like common sorrel, have seeds which some birds eagerly feed on. Brightly coloured goldfinches have been taking advantage of the burgeoning seed source.  In July there were several family groups in evidence around the Abbey and come winter the longer grass will provide cover and feeding for ‘charms’ (the lovely collective noun for a group of goldfinches) as they gather in winter flocks. They can balance and feed on the slimmest of perches, and are a delight to see feeding and flying around the Abbey. 

The goldfinch, a ‘charming’ visitor at any time

Staying on the theme of birds, corncrake was recorded calling from within the Abbey grounds this summer by colleagues working for the National Trust for Scotland. The long grasses behind the Abbey grounds were providing cover for this shy bird, which breeds in the fields close by. 

Another interesting record this year saw common lizard logged, these were sighted on the rocks and taking advantage of the plentiful long grass cover.

Behind Iona Abbey the long grass is being used by calling corncrakes

The grassland changes and pleasing visual impact is bringing about a nice cultural change from both visitors and colleagues.  As many a local authority will testify, it’s not an easy ride changing grassland management practices. The ‘practicalities’ of meadow management can throw up challenges in terms of equipment, knowledge, and perception. However, at HES, we are hoping that the thoughtful and incremental changes seen at Iona Abbey will, in time, make a positive impact on our estate as a whole.  

Find out more about Historic Environment Scotland’s grassland revolution and similar works carried out at Dryburgh Abbey.

© Historic Environment Scotland.

Architecture & Design Digest

By Athayde Tonhasca

Honey bees and bumble bees are familiar to most people and deservedly valued for their ecological and economical importance. These bees are social species; they live in colonies comprising female workers that collect food, take care of the brood and guard the nest, and a queen, who’s mostly responsible for egg-laying (males are sporadically produced and have short lives). Despite their standing among us, honey bees and bumble bees are not the best representatives of the over 20,000 known species of bees. More than 75% of them don’t live in a colony: instead, each female bee constructs her own nest and provides food for her offspring. And an estimated 60 to 80% of species are fossorial (from the Latin fossorfor ‘digger’), that is, they are burrowing animals that spend a significant part of their lives underground. These bees build subterranean nests where their immature stages complete their development. Some bumble bees also nest underground, but they are superficial diggers; fossorial bees excavate burrows deep down, and for that reason they are known as mining bees.

There are many types of mining bee nests, but a typical design comprises an entrance surrounded by a small ‘volcano’ of excavated soil, known as a tumulus. This entrance leads to a tunnel, which may branch into cells. The female will stock each cell with a ball of pollen and lay an egg on it. The larva will feed on the pollen until it is ready to emerge as an adult.

Nest diagams of the mock-orange miner bee (Andrena candida) © Youssef & Bohart, 1968.

Compared to the social species, we have scant information about the much more diverse solitary mining bees. But we do know that many species are essential for the pollination of crops and wild plants, so solitary bees are increasingly being taken into consideration in management plans for pollinators. One aspect however often goes unnoticed: bees’ housing needs. 

When a female bee finishes provisioning her nest, her offspring are on their own. Their survival depends on mum’s ability to stock sufficient high-quality food, and also on her skills in building a nest that is safe and sturdy. For that, not just any spot on the ground will do: the soil must have a range of properties that allow a bee to excavate easily and efficiently, while at the same time maintaining the nest structure intact. Few bees tackle these engineering challenges as efficiently as the alkali bee (Nomia melanderi).

An alkali bee nest. Illustration by Julie Johnson (Life Science Studios) © Kapheim et al., 2021.

The alkali bee is a native to deserts and semi-arid areas of the western United States where it collects pollen from a variety of plants, including alfalfa (Medicago sativa). Just like our heather colletes (Colletes succinctus), the alkali bee is gregarious; females build their individual nests close to one another, sometimes forming enormous aggregations. This bee quietly helped alfalfa growers in the American West for many years, but its services were only noticed when farmers in Utah intensified their operations by using pesticides and ploughing over alfalfa beds. As a consequence, alfalfa yields plunged. Researchers quickly learned that the alkali bee is much more efficient than the European honey bee (Apis mellifera), until then supposedly the main pollinator of alfalfa (thanks largely to the alkali bee’s tolerance for being whacked on the head when the flower is tripped).

A female alkali bee by her nest. Photo by James Cane © United States Forest Service.

Researchers also determined that the alkali bee chooses nesting sites with salty surfaces free of vegetation, and the subsoil moisture must be just right: if too dry, the larvae dry out; if too wet, mould spoils the pollen provisions. After learning about the bee’s nesting needs, alfalfa growers, especially in the Touchet Valley, Washington State, have been building alkali bee nesting beds adjacent to alfalfa fields for over 60 years. These beds consist of a waterproof base and layers of gravel and sand; buried pipes supply the right combination of water and salt. These actions are quite effective: a 1.5-ha nesting bed grew to 5.3 million females (353 nests/m²), the largest bee nesting aggregation ever recorded (Cane, 2008). These bees are abundant enough to change the landscape: in one year, a population estimated to be 9.1 million-strong brought 96 tons of soil to the surface as a result of excavation work. Much of this earth is eroded away by wind and rain, which would result in a loss of 4 cm of soil surface in 50 years (Cane, 2003). But farmers are not complaining: they get about 2,200 kg/ha of clean alfalfa seed, as opposed to 168 kg/ha without the alkali bee. 

An alkali bee bed at the edge of an alfalfa field © Jim Cane, United States Department of Agriculture.

The alkali bee is a case study about the importance of nesting sites for the success of mining bees, although we know far less about most species. Nonetheless, a range of studies and observations give us some guiding principles.

Soil texture, which expresses the relative amounts of soil particles – sand, silt and clay – seems to be the main factor determining site selection. Texture regulates moisture content, temperature and aeration, all important factors for brood survival. It also greatly determines whether the soil is too hard or too soft; if too hard, bees may spend a lot of energy digging, sometimes unsuccessfully. This wasted effort may contribute to up to 80% mortality of female bees during nesting. But if the soil is too soft, the nest may collapse or be more vulnerable to predators.

The orange-legged furrow bee (Halictus rubicundus) has adapted well to variations in soil texture and compaction. This species tends to nest alone where the season is short (high latitudes or high elevations) or in aggregations elsewhere. Where they aggregate, they build their nests in soft soils if the population is low. But aggregations with high density of nests are established in harder, more compacted soils. This seems to be a trade-off between efficiency and structural integrity; the going is easy in soft soils, but nests may collapse if there are too many of them (Potts & Willmer, 1997). As far as we know, most mining bees don’t have the orange-legged furrow bee’s flexibility for soil textures. Of the species investigated, the large majority need soil classed as sandy or sandy loam (which is mostly sand with some silt and a smaller amount of clay).

Soil types: important factors for farmers, civil engineers and mining bees © cmglee, Wikimedia Commons.

Temperature also plays an important part in bees’ choice of nesting sites. Most of the species studied look for areas of bare or sparsely vegetated ground, which are more exposed to the sun and therefore warmer than soil obscured by plants. A terrain sloped towards the south (in northern places) is even better, because these situations also maximise the absorption of solar radiation. Many ground-nesting bees go even further: they nest on embankments or any steep, near vertical surface to take full advantage of insolation. The orange-legged furrow bee and some related species (family Halictidae) use another trick to keep their homes warm and cosy: they prefer to nest near or under pebbles and stones, which absorb and retain heat. Nests constructed under stones can be 2-3°C warmer at a depth of 5 cm than bare soil (Packer et al., 1989).

A female orange-legged furrow bee, a master engineer © linsepatron, Wikimedia Commons.

We have a long way to go in understanding mining bees’ nesting requirements. We have limited information for a fraction of the species, and some of them don’t toe the line. The sharp-collared furrow bee (Lasioglossum malachurum) for example, pollinator of a range of plant species across Europe and northern Africa, nests in hard, horizontal ground with or without vegetation cover. Its main requirement is alkaline soils (Polidori et al., 2010).

A female sharp-collared furrow bee: a species that goes against the trend for nesting sites © Gideon Pisanty, Wikimedia Commons.

Nonetheless, there have been successful attempts to come up with management prescriptions. Based on bees’ general preference for open ground, Nichols et al. (2020) used farmyard machinery to scrape bare areas on farmland in Hampshire, UK, to see whether these plots would become nesting grounds. The answer was ‘yes’: nests of the short-fringed mining bee (Andrena dorsata) and at least three other species were more abundant in bare soil than in control areas. In Britain, the short-fringed mining bee is one of the main flower visitors of apple (Malus domestica), field bean (Vicia faba), oilseed rape (Brassica napus) and strawberry (Fragaria x ananassa), which are the most important orchard, protein, arable, and soft fruit crops, respectively (Hutchinson et al., 2022). So, some light farmland engineering could significantly improve yields.

Red circles mark nest entrances in a soil scrape © Nichols et al., 2020.

There has been a growing realisation that housing is as important as food to support bees and other flower-visiting insects. Understanding nesting characteristics of the secretive mining bees is not an easy task, but the more we strive for it, the more we safeguard their pollinating services.

Master manipulators

By Athayde Tonhasca

When the headmaster of a German grammar school became ill because of problems with unruly students, their well-off parents and school supervisors, his doctor recommended the study of nature to relax and deal with stress. This scenario would be painfully familiar to many teachers today, but the headmaster in question was Christian Konrad Sprengel (1750-1816), who took up the doctor’s advice and became one of world’s greatest botanists (Zepernick et al., 2001). Among many contributions, Sprengel proposed that the main purpose of flowers was to attract insects for achieving sexual reproduction via pollination. Sprengel also discovered that some orchid flowers lure pollinators without offering pollen, nectar or any other reward. In other words, those orchids rely on deceptive Scheinsaftblumen, ‘sham nectar flowers’.

A commemorative stone in Berlin’s Botanical Gardens, based on the frontispiece of Spengel’s seminal work on plant reproduction © Rüdiger, Wikimedia Commons.

Sprengel’s idea of deceptive flowers didn’t settle well with contemporary fellow naturalists, who maintained that the diversity and abundance of angiosperms (flowering plants) depended on their mutualistic relations with pollinators; any cheating would pull to pieces these fine-tuned interactions. Darwin wrote that anyone who believed in ‘so gigantic an imposture’ must ‘rank the sense or instinctive knowledge of many kinds of insects, even bees, very low in the scale’. But it turns out that insects do fall for impostures; an estimated 4 to 6% of all flowering plants use some form of trickery to lure pollinators. They most commonly do that by food deception, falsely advertising pollen or nectar by their flowers’ shape, colour, scent, or pollen-like structures. Plants can also resort to sexual deception, when flowers look or smell like female insects, luring males to a non-existent partner, or some other ruse.

Orchids are famed cheats; about one-third of the roughly 28,000 known species attract pollinators with a variety of subterfuges, giving back nothing. But despite their intricate adaptations to mislead pollinators, orchids are amateurs when compared to sophisticated schemers in the plant world such as the parachute or umbrella plant (Ceropegia sandersonii, family Apocynaceae), a native of southeast Africa and a houseplant elsewhere. 

A parachute plant © Wouter Hagens, Wikimedia Commons.

When a European honey bee (Apis mellifera) approaches a flower, it risks being pounced upon by a predator, especially crab or flower spiders. If the bee is not alert or fast enough, it will find itself in the spider’s palps. The ensnared bee releases defence pheromones (volatiles that elicit a reaction from members of the same species) to alert sister bees. Those chemicals can also be picked up by another creature altogether: a jackal fly, aka freeloader fly (family Milichiidae). Some of these small, dark, widespread but poorly known flies are kleptoparasites – ‘parasites by theft’, which steal food from another animal, like frigate birds and hyenas. As the spider’s lunch struggles hopelessly to free itself, jackal flies come out of nowhere to land on the bee and feed on the substances oozing from its body – they possibly also pierce the honey bee ‘skin’ (exoskeleton) to get its juices. You can watch them in action here. If the jackal flies don’t respond quickly to the bee’s chemical cues, they will miss the opportunity to get their share before the spider finishes its meal. 

A honey bee having a bad day: captured by a crab spider, it releases alarm pheromones and other volatiles that attract jackal flies © JonRichfield, Wikimedia Commons.

In a remarkable selective twist, flowers of the parachute plant produce a mixture of chemical compounds that include some of the very volatiles released by European honey bees when they bite or sting to defend themselves against attackers. Such chemicals are not going to entice bees or most other pollinators to visit the flowers, but they are irresistible to jackal flies. As it turns out, these flies are the main pollen carriers of the parachute plant (Heiduk et al., 2016). This chemical stratagem seems overly elaborate, but the parachute plant is not alone is deploying it.

The round-leaved birthwort or smearwort (Aristolochia rotunda) is a herbaceous plant native to Southern Europe. Oelschlägel et al. (2015) discovered that its flowers release volatiles of the type found in other angiosperms, but also some chemicals identical to those produced by true bugs of the family Miridae when they are attacked by spiders, ants, praying mantis or any predator fancying a juicy meal (while the term ‘bugs’ is used for insects in general, true bugs are insects in the order Hemiptera: cicadas, aphids, leafhoppers, shield bugs, etc.). ‘Volunteer’ mirid bugs squeezed with a forceps quickly attracted flies, most of them frit flies (family Chloropidae). And just like the jackal flies, these frit flies are kleptoparasites: they feed on – you may have guessed it – on the exudates of dying or freshly killed bugs. And crucially for our tale, frit flies are drawn to the flowers of round-leaved birthwort in its natural habitat and end up carrying away nearly 90% of the pollen produced. 

L: a round-leaved birthwort flower © Kenraiz, Wikimedia Commons; R, top: the frit fly Trachysiphonella ruficeps carrying round-leaved birthwort pollen on its head and thorax; R, bottom: T. ruficeps flies mobbing a freshly killed Capsus ater mirid © Oelschlägel et al., 2015.

Almost all known Aristolochia species use deception and are myophilous (pollinated by flies); more specifically, these plants rely on either sapromyophily, which is pollination by flies that are attracted to the scents of dead animals or dung, or micromyiophily, which is pollination by the smallest flies. The authors of the birthwort study proposed a new term to describe pollination carried out by kleptoparasitic flies: kleptomyiophily (you may wish to keep these and other pollination syndrome terms handy to ace your next Scrabble match).

The parachute plant and the round-leaved birthwort dupe their kleptoparasitic pollinators with smells, but the rare Ceropegia gerrardii (family Apocynaceae) from eastern South Africa made things a bit fancier. Instead of scents alone, its flowers secrete a liquid containing protein and sugars which is similar to the ‘blood’ (haemolymph) of injured honey bees and other insects. These ‘bleeding flowers’ are irresistible to jackal flies hoping to find a vulnerable, dying honey bee – so in this case, pollinators are rewarded. The combination of scent and free ‘blood’ encourages the flies to stick around and feed for longer, thus increasing the chances of pollen contamination. And the trick seems to work: among all visiting flies, almost all pollen carriers were females of four kleptoparasite species in the genus Desmometopa (Heiduk et al., 2023).

(a) C. gerrardii flower with droplets secreted by the corolla lobes; (b) a corolla lobe covered with secreted liquid; (c) fly ready to remove or deposit a pollinarium; (d) fly lapping the secreted liquid; (e) fly holding a blob of secretion. Arrows in (d) and (e) indicate a pollinarium attached to the fly’s mouthparts. Bars: (a) 5 mm, (b) 2 mm, (c) 0.6 mm, (d) 0.3 mm, (e) 0.4 mm © Heiduk et al., 2023.
 

It would be worth a moment to appreciate the plants’ achievements in resorting to deception by kleptomyiophily. They don’t rely on flowery bouquets or sexual decoys, which may trick run-of-the-mill visitors that may have questionable pollination abilities. Instead, by mimicking the chemical signature of doomed insects, these plants manage to dupe a cohort of fast-responding, highly specialised and efficient pollinators that otherwise would have no interest in visiting their flowers. It’s had to beat that for cunning manipulation.