Readers’ wildlife photos

Today’s story-plus-picture piece, with a very cool story on pollination, comes from Athayde Tonhasca Júnior, whose notes are indented. Click on the photos to enlarge them.

Master manipulators

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, pollination by flies that are attracted to the scents of dead animals or dung, or micromyiophily, 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.

JAC:  As Leslie Orgel said, “Evolution is cleverer than you are.”  This is an amazing series of evolutionary tales—and appropriate for Halloween.