New paper: The whimsical long-proboscid fly and its favourite colour.

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The flowers on one of these plants conceal drops of sticky nectar. The other is a cheating orchid, presenting empty flowers and false promises. Can you tell which is which? Even if you knew which one carried nectar, how can you tell the difference between them? The two plants might look a bit different to human high-res optics, but now try blurring your eyes. Pretty similar, huh?

What about this pair?

Screenshot 2018-10-30 15.09.50If it’s difficult for our brains and eyes to discern the difference between the flower with the reward and the one that’s falsely advertising, then what hope does a nectar-hunting fly with low resolution compound eyes and a smear of a central nervous system have?

Specifically, I’m talking about this fly…

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If this fly looks embarrassed, its because it has orchid pollen stuck to its face.

Until now, you probably thought lion, or elephant, or rhino were the most impressive animals roaming the grasslands of southern Africa. Well you’re wrong, and it’s ok to change your mind after seeing the majestic long-proboscid fly of South Africa. There are several species of these magnificent beasts, and this one is named Prosoeca ganglbaueri.

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That giant proboscis hanging from its face is a tool crafted by evolution for sucking nectar from the bottom of long flower tubes, and it can grow as long as 5 cm (which is longer than the fly’s own body length). Unlike butterflies who coil their proboscises, the long-proboscid flies simply hinge the instrument down, tucking it away underneath their bodies to trail out behind them. And this species isn’t even the most extreme: proboscises in Moegistorhynchus longirostris get up to 8 cm!

Sometimes handling that long instrument can be a challenge…

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In some areas of South Africa, P. ganglbaueri is the only creature capable of extracting nectar from flowers with very long floral tubes, and because of this it has become the exclusive pollinator for 20 species of plant. Altogether, the long-proboscid flies as a group bear the great responsibility as the only pollinator for approximately 130 species of plant, making them a truly important creature for the ongoing survival of many South African plants.

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Figure 1 from Whitehead et al. (2018): Prosoeca ganglbaueri feeding from a variety of nectar sources. (a) Zaluzianskya microsiphon, (b) Scabiosa columbaria, (c) Agapanthus campanulatus, (d) Dianthus basuticus.

An interesting fact about flowers that are pollinated by long-proboscid flies, is that most of them are pink, or white, or some variation in between (with one blue exception). This strong colour preference is a critical feature directing the evolution of the cheating orchid flowers introduced earlier. For a deceptive orchid to attract this fly, the orchids’ flower colour must match the flies’ colour preference, or the mimicry simply won’t work.

In my recent paper, we asked whether the colour preference of flies was something that they learned, like we learn to associate that perfect golden-brown hue of fried food with a mouth-watering culinary experience, or if it was instead a more hardwired innate response, like a moth drawn to a lamp. The answer is important for understanding ultimately what is driving the evolution of false advertisement signals in mimic orchids. So, for example, if flies had an innate bias to pink or white, then cheating orchid flowers would evolve to match that bias, in the same way that any good advertisements are designed to appeal to the fundamental desires of its audience. On the other hand, if flies learned to associate nectar reward with certain colours, their preference should be determined by the colour of their local nectar diet. Under the learned scenario, orchids should be evolving to match local flowers’ colours, not any intrinsic bias of the fly.

To test this, I took advantage of just how easy it is to bamboozle these flies. With a home-made artificial flower, painted to match the pink and white flowers visited by the fly, anyone can fool a fly into attempting to feed. So I mounted a pink and a white model to my “interview stick”, and travelled across the rugged Drakensberg Mountains to interview various populations of flies. In each location, I recorded whether the local flies preferred probing the pink or white model flower, as well as the colour and species of flower that the flies were using for nectar there.


The results were clear. Flies used to feeding mainly on pink flowers preferred the pink model. Flies that fed mainly on white flowers preferred the white model. And flies that fed on both pink, white, and violet flowers, showed no clear preference between pink and white.

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Figure 3 from Whitehead et al (2018): Pink-white preference for flies at seven sites. The x-axis shows colour preference, with pink on the right, white on the left. Measured preference at seven sites is represented, with the colour of local nectar sources depicted in the small pie charts.

This tells us that the flies are very flexible in their preferences, and the strong implication is that these flies are learning to associate colour and reward. A further result showed that as the variation of colours flies fed from increased, this made them less choosy in the pink-white preference choice. So the bottom line is that the colour of their local nectar-buffet strongly controls a fly’s colour preference.

What does this mean for orchid cheats? Well, the colour of nectar cheats is all important, and what matters most for the success of a deceptive orchid is the colour composition of the surrounding nectar-rich floral community.

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Post-script:
Still wondering about which flowers in the opening images were cheats, and which had nectar?

In both cases the deceptive orchid is on the left. The first image features Disa nivea (left), and Zaluzianskya microsiphon (right), the second features Disa pulchra (left) and Watsonia lepida (right).

Reference:

Whitehead MR, Gaskett AC, Johnson SD. (in press) Floral community predicts pollinators’ color preference: implications for Batesian floral mimicry. Behavioral Ecology 

Sex, lies and pollination. Australia’s remarkable sexual swindlers.

Article reposted from original publication with The Territories.

Rather than luring its pollinator with the promise of food this flower uses an equally, if not more, powerful motivator: sex.

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In shades of dusky green and claret red, the bird orchid’s subdued palette hints at its alternative lifestyle. The usual strategy for flowers attempting to catch the compound eye of a passing insect is to advertise proudly. Petals are used as panels for saturated colour, assembled en masse into conspicuous aggregate displays exuding exotic scents. In this way, nectar-filled flowers loudly broadcast the promise of their reward to entice would be pollinators into servicing them.

 

A deviant among flowering plants, the bird orchid eschews these typical hallmarks of floral advertisement. Crouched modestly on the forest floors of eastern Australia, its stature belies its status as one of the supreme specialists amongst the world’s flowering plants. Like those other showy flowers, the bird orchid needs the service of a pollinator from time to time, however unlike most other flowers, it attracts its pollinator without the payment of any reward. The orchid flower in fact completely lacks nectar.

 

Rather than luring its pollinator with the promise of food this flower uses an equally, if not more, powerful motivator: sex. Undetectable to human senses, the orchid’s advertisement is a precise chemical mimicry of a female wasp’s sex pheromone. This is targeted marketing at its finest, as the use of a signature sex pheromone ensures that the orchid attracts only males of a specific species of wasp.

 

Skimming by on wide zig-zagging flights, the wasps are interminably attracted when the ruse takes hold. They alight onto the flower with fervor, probing and hunting for the mate that their senses scream must be there. Bucking back into the column of the flower (the reproductive parts of an orchid flower are fused in this special structure), they make contact with the anthers and a large packet of pollen is deposited on them. The wasp disengages eventually and leaves, but soon, elsewhere, he will catch on the breeze the smell of a mate, and if fooled again, fulfill his role as duped courier for an orchid’s reproductive ends.

 

Called “sexual deception”, this mode of pollination was noticed by Darwin and his contemporaries in an age in which Europe’s natural sciences were in full bloom. It was a naturalist in Blackburn, Victoria however, who was first to discover the phenomenon outside Europe. In 1927, Edith Coleman had turned her great capacity for observation of the natural world to a peculiar native orchid. Resembling more flesh than flower, Cryptostylis, known also as “tongue-orchids” had caught her attention for its magnetic allure to a specific kind of wasp. Through her observations, Coleman was able to discern that male wasps were being attracted to the flower in order to copulate with it. An experiment through a window showed scent to be the primary attractant, and Coleman even observed the ejaculate remaining after having been visited by clearly convinced wasps. She wrote up her notes in a series of papers for the Victorian Naturalist and Transactions of the Royal Society for Entomology, which made quite a splash with the best of botany at the time.

 

We now know this was the tip of the iceberg. Australia is not only home to tongue orchids, but hosts a diverse array of other sexually deceptive orchids including the spider orchids, elbow orchids, hammer orchids, dragon orchids, greenhoods, duck orchids, hare orchids, beard orchids, bird orchids, and the list goes on. Harbouring over 50% of the world’s known examples of sexually deceptive pollination, Australia is certainly the world’s hotspot for this unusual phenomenon. Remarkably, we have several hundred species that employ this unique brand of pollinator attraction, and what is more remarkable, the evidence points to at least six different independent evolutionary occurrences in the Australian orchid family tree. To our eyes, sexual deception seems like a freaky, unlikely strategy and its repeated independent incidence through Australia’s evolutionary history is therefore a startling paradox.

 

Although the reliance on a single species of pollinator for pollination seems precarious, studies have demonstrated that sexual deception comes with the advantage of promoting healthy breeding for our native orchids. In nectar-bearing plants, foraging insects will frequently move between flowers on the same plant and between neighbouring plants. Called “optimal foraging”, exhausting local nectar supplies in a patch before putting energy into finding a new buffet makes economic sense for a nectar-feeding insect. Sexual deception however, has been shown to drive pollinators far from the flower after being fooled, so that pollen escapes the local neighbourhood. As a plant, your neighbours are likely to be related to you, thus deception is a way of ensuring offspring quality by avoiding breeding with your relatives.

 

Another factor supporting the profusion of our sexually deceptive species is Australia’s immense diversity of insects to fool. Although there are examples of gnat and ant sexual deception systems, wasps are the most commonly targeted pollinator for our orchids. Incredibly, we are only now beginning to uncover the immense hidden diversity of Australian wasps. For example, a recent study in a small patch of bush near Margaret River uncovered 28 species of wasps, most of which were previously unknown to science. With each of these species most likely having their own private sex-pheromone cocktail, there is seemingly a kaleidoscope of chemical communication channels available for different orchids to exploit.

 

Despite our deepening understanding of the natural history of sexual deception, its repeated occurrence in Australia remains a true puzzle.

 

Try the Atlas of Living Australia’s region search to discover which orchids (Plant family: Orchidaceae) live near you. [Link: http://biocache.ala.org.au/explore/your-area%5D