The sun is setting on another day in the field, and I’m once again lying prostrate at the altar of The Orchid. The object of my worship: a tiny swan greenhood orchid about 10 cm tall, growing inconspicuously through the surrounding grasses. In the fading light, I need the help of an LED light panel to gently illuminate the small plants which will be my study species for the next three weeks.
I’m camped out at Terrick Terrick National Park in northern Victoria. The Park is a mix of Callitris (cypress pine), open grassy Eucalyptus woodland and herb-rich native grassland. The campground is situated at the base of Mt Terrick Terrick, a large granite outcrop which overlooks the surrounding countryside. Before European colonisation, the Dja Dja Wurrung peoples used the rocky outcrops as a shelter and home. From the top, there is a 360° uninterrupted vista over the surrounding plains, and I get the distinct feeling that this is a place of special significance.
My mission, though, was to find out how the swan greenhood (Pterostylis cycnocephala) was pollinated.
The view from Mt Terrick Terric looking west at sunset.
Imagine, for a moment, that you’re a male fungus gnat. You’re small, maybe 3 mm long, with two black wings. You’ve spent the last three weeks as a small maggot, breaking down organic matter and feeding up for the moment you can finally be released to find a mate. The weather has just started to warm up, and you’ve emerged feeling horny.
All of a sudden, you smell something irresistible. A female. You’re on! You fly as close as you can, weaving backwards and forwards to hone in on the chemical trail leading you to your new mate. You land on a bit of vegetation and quickly run around to find her.
There! You spot her. You wave your wings to let her know you’re keen. She looks and smells AMAZING. You do your moves and she doesn't run away. Things are looking promising. You get ready to do the deed, grasp on to her genitalia and twist around to the normal mating position when…
BAM! and you’re catapulted into a trap. You’re unhurt but very confused. What went wrong?! You struggle around and try to escape but its a confined space. Eventually you work out that there is a small escape pathway which you squeeeeze your way through. You brush past something sticky but manage to escape out to the open air.
What the hell just happened?! You notice you’ve picked up an uncomfortable item on your back, like a bright yellow high-vis rucksack. You shrug. Oh well, what can you do. Back to the task of finding a mate…
And that is how the swan greenhood manages to transfer pollen from one plant to another - on the back of males of a single undescribed species of Bradysia from the diverse fungus gnat family Sciaridae.
This type of pollination is known as pollination by sexual deception. Pollination by sexual deception is rare in plants, but some orchids have become masters of pretending to be female insects. The orchid manages to deceive the male gnat by emitting chemicals which are probably the same (or very similar) to those produced by the female insect to attract a mate. These chemicals are crucial to attract males to the flower.
Once the male gnats arrive at the swan greenhood flower, the blackish labellum appendage acts as a female dummy, and the male gnat is duped into attempting to mate with it. Once the gnat has completed its copulating manoeuvre and twisted to face downwards, the labellum is triggered and flips upwards to trap the gnat inside the top of the flower. From there, the male gnat must squeeze through a pair of column wings to escape, picking up pollinia on its thorax as it exits through the front of the flower.
An illustration of the floral morphology of the swan greenhood, Pterostylis cycnocephala. (A) the whole plant, (B) flower details, (C) inside of flower showing trap mechanism with the trap set and labellum in the open position, (D) labellum triggered in the closed position. Scale bars are 10 mm.
Stills from a video of a male Bradysia sp. gnat becoming trapped and removing pollinia. (A) approaching the labellum while wing fanning; (B) curling abdomen through legs; (C) grasping labellum appendage with genitalia; (D-E) twisting away through 180° to face downwards; (F-G) labellum triggers and gnat is trapped; (H) carrying orchid pollinia. Scale bars are 1 mm.
I was interested to know a bit more about how this interaction works. How exactly does the orchid fool the gnat?
To do this, I conducted a series of dissection experiments. By cutting and manipulating various parts of the flower, and seeing how the gnats responded, I could understand more about how the system works.
First, I constructed a paper shield and presented the shield for 10 minutes before adding flowers inside the shield for a further 10 minutes. This way, gnats couldn’t see the flowers, but they could smell them. I found that male gnats ignored the paper shield, but when I hid flowers inside the paper shield, they responded quickly, confirming that chemistry is important in attracting male gnats to flowers.
Next, I cut the labellum from the rest of the flower, and presented the labellum alone, and the rest of the flower alone. The combination of the labellum and the rest of the flower was my control. I found that gnats only responded to the rest of the flower, indicating that the chemicals which attract the males are produced in the rest of the flower and not in the labellum. However, male gnats responding to the rest of the flower displayed much lower sexual behaviour and didn’t attempt to mate with the flower. With the labellum added in the control, they again attempted to mate with the labellum appendage.
So, the chemicals attract the gnats to the flowers, but perhaps the appendage was important in encouraging copulation attempts.
To test if this was due to chemicals produced only in the appendage, or because the appendage looked and felt like a female gnat, I conducted another dissection experiment. This time I cut the labellum and pinned it to the flower in such a way that the appendage was hidden from view inside the trap part of the flower. I also cut the labellum of another flower and pinned it in such a way that the appendage was visible and accessible (my control). I found that male gnats only tried to copulate with the flowers where the appendage was visible and accessible, even though they would have been able to smell the appendage when it was hidden. Therefore, I concluded that the shape and/or colour of the appendage are likely to be important, rather than just the smell.
In other words, good smell and good looks are required to deceive the male gnat.
This research was published as an article in the Botanical Journal of the Linnean Society in 2022. The link to the article is here: https://academic.oup.com/botlinnean/advance-article-abstract/doi/10.1093/botlinnean/boac015/6574694. The article is subscription only, meaning you (or your institution) needs to be subscribed to the journal. If you would like a copy of the paper, feel free to email me at tobiashayashi@hotmail.com.
Hayashi T, Reiter N, Phillips RD, Peakall R. (2022) Sexual deception of male Bradysia (Diptera: Sciaridae) by floral odour and morphological cues in Pterostylis (Orchidaceae). Botanical Journal of the Linnean Society.