Menacing tenants

By Athayde Tonhasca

In an apple orchard somewhere in the American state of Pennsylvania, an adult Japanese horn-faced bee (Osmia cornifrons) has just emerged from its nest and makes its way into the big wide world. The apple grower has high hopes for that bee; in fact, he bought many of them when they were still inside their cocoons. The Japanese horn-faced bee was introduced from Japan in the 1970s, and since then it has been widely used in the Eastern United States to improve the pollination of apples and other fruit trees such as peaches, pears and cherries.

A female Japanese horn-faced bee © Chelsey Ritner, Exotic Bee ID.

In their natural habitats, the Japanese horn-faced bee and similar species such as the red mason bee (O. bicornis) nest inside natural cavities such as hollowed reeds, tree holes and cracks in stones. Females use a range of materials, especially mud and pebbles, to build individual nest cells in which they lay an egg. When bees are done, they seal off the nest entrance with mud – so they are known as mason bees. Fruit growers offer bees nesting alternatives such as drilled blocks of wood or bunches of cardboard tubes tightly packed together.

Two types of mason bee nests used in orchards: cardboard tubes (a) and wood blocks (b). Pictures by N. Joshi © Kline et al., 2023.

The future seemed promising for that Japanese horn-faced bee in Pennsylvania. But opportunists were on standby, ready to pounce when an unsuspecting bee leaves its nest. In the blink of an eye, a gang of hypopi (singular hypopus) jumps on the bee, holding on for dear life as their ride flies away.

Hypopi, also known as hypopodes, are a special nymphal stage found in some mites. In this case, the hairy-footed pollen mite (Chaetodactylus krombeini). Hypopi have no head or mouthparts, but are armed with special structures for hanging on; either powerful claws or a sucker plate to glue themselves to their host. These adaptations greatly facilitate phoresis, which is when an organism attaches itself to another for the purpose of transportation. Phoresis is typically found in small and poorly mobile organisms such as nematodes and mites. But curiously, the hypopus stage is usually facultative for mites; it occurs only when conditions deteriorate (food scarcity, overcrowding, dry climate, etc.), so that skedaddling increases the likelihood of survival.

A hypopus, the stage adapted for phoresis © Reynolds et al., 2014.

The departing bee has no chance of avoiding the lurking hitchhikers who react instantaneously to the slightest touch to their dorsal setae (bristles) or to air movement caused by a passing body. And the feats of some of these mites defy credulity; the tiny Histiostoma laboratorium (formally known as H. genetica), a scourge of vinegar fly (Drosophila melanogaster) laboratory colonies, lurches into the air to grab fruit flies flying above them (Hall, 1959. J. Kansas Entomological Society 32: 45-46). Some species that have hummingbirds as hosts rush to the birds’ nostrils at a rate of 12 body-lengths per second, which is a speed similar to a cheetah’s (Colwell, 1985)

Hypopi attached to their host © D.E. Walter, Invasive Mite Identification, Colorado State University and USDA/APHIS/PPQ Center for Plant Health Science and Technology.

After being mobbed by hypopi, the bee carries on with its life. If it’s a female, she will mate and start a nest of her own. When her brood cells are ready, her unwanted companions come out of their lethargic state, jump off and resume their development, maturing and reproducing very quickly, all the while feeding on the pollen and nectar gathered by the bee. When their numbers reach certain levels, they may feed on the bee’s eggs and larvae (details are sketchy). In a few months the mites may reach thousands and overrun the brood cell, leaving space for nothing else.

Hairy-footed pollen mites inside a mason bee nest cell © Pavel Klimov, Wikimedia Commons.

Such massive numbers of kleptoparasites (organisms that steal food from another one) spell serious trouble for Japanese horn-faced bees; their eggs and larvae die or develop poorly for lack of food or direct attack from mites. Some adult bees may not even have a chance to start a new family; they may be so burdened by mites that they cannot fly. They fall to the ground and become easy pickings for ants and other predators.

A mason bee loaded with pollen mites © GeeBee60, Wikimedia Commons.

Several mason bee species are susceptible to the hairy-footed pollen mite, but managed Japanese horn-faced bees have been hit particularly hard, with losses reaching up to 50% of the population. It’s not difficult to understand why. The same way slum housing conditions make people more vulnerable to all sorts of diseases, jam-packed nests increase the chances of mites passing from one bee to another. And the hairy-footed pollen mite does not even depend on phoresis: adults can walk from one nest to another nearby, getting inside through holes in the sealing mud made by parasitic wasps. To make the situation worse, this mite can turn into a dormant stage that survives several years inside an empty nest, rousing back to activity as soon as new tenants arrive.

The effects of the hairy-footed pollen mite on the Japanese horn-faced bee are a reminder of the unintended consequences of well-intentioned actions. Bee houses or bee ‘hotels’ have been promoted as enhancers of wild bee populations, but there’s no indication of such effects. They do however increase the risk of pathogens and parasites: not only mites, but a range of fungi, parasitic flies and wasps bedevil mason bees (Groulx & Forrest, 2017).

A bee hotel: not such a great idea © Colin Smith, Wikimedia Commons.

American fruit growers do their best to keep mites under control by replacing the nesting tubes yearly, sterilising wood blocks, or removing and storing bee cocoons during the winter. If you have a bee house but don’t have the resources, time or inclination to do the same, you should follow Colin Purrington‘s advice: buy a garden gnome instead.

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.