Credit: Credit: T. Rupp, B. Oelschlägel, K. Rabitsch et al.

The plant Aristolochia microstoma uses a unique trick: its flowers emit a foul-smelling, musty scent that seems to mimic the smell of decomposing insects. Flies out of the genus Megaselia (Family Phoridae) are likely to be attracted to this smell when looking for insects to mate and lay their eggs in. When they step into a flower, they become trapped and first pollinate the female organs before being covered with pollen by the male organs. The flower then releases them unharmed.

“Here we show that the flowers from A. Microstom emit an unusual mixture of volatiles, including alkylpyrazines, which are otherwise rarely produced by flowering plants. Our results suggest that this is the first known case of a flower that deceives pollinators by smelling of dead and rotting insects rather than vertebrate carrion, ”says the corresponding author Prof. Stefan Dötterl, head of the plant ecology group and of the Botanical Garden in Paris. Lodron University Salzburg, Austria. The study will be published in the Open Access Journal Limits in ecology and evolution.

Between 4 and 6% of flowering plants use a “deceptive pollination strategy”: they use smell, color and touch to reward pollinators such as nectar, pollen or mating and breeding grounds, but they do not. The deception works because pollinators are unable to distinguish between reward and imitation. Deceptive pollination is typical of many orchids but has evolved independently in other plants as well, including in the genus Aristolochia (family Aristolochiaceae or Birthworths).

“Aristolochia contains over 550 species worldwide, especially in the tropics and subtropics. It is mainly woody vines and herbaceous perennials with striking, complex flowers that temporarily lock visitors in for pollination, ”says Prof. Christoph Neinhuis, co-author of the study, who cultivates one of the largest Aristolochia collections worldwide at the Botanical Garden of the TU Dresden .

When pollinators enter an Aristolochia flower, hairs lead them down into a small chamber where the genital organs are located. Trapped inside, they deposit pollen that they carry on the female organs before the stamens mature and release more pollen. When the hairs blocking the entrance to the chamber wither, the pollinators can escape and a new cycle can begin.

“It is known that many Aristolochia species attract flies with floral scents that imitate, for example, the smell of carrion or feces of mammals, rotting plants or fungi,” says first author Thomas Rupp, doctoral student at the University of Paris-Lodron in Salzburg. “But our curiosity was aroused by A. Microstom, a species known only from Greece: in contrast to other Aristolochia with its striking flowers, A. Microstom has inconspicuous brownish flowers that are horizontal, partially buried or close to the ground between leaves or rocks. The flowers release an unpleasant, carrion-like odor that is noticeable to people at a short distance. “

Rupp and colleagues tried A. Microstom Plants from three locations in Greece: one west of Athens and two in the Peloponnese. From 1457 flowers (72% of which were in the first female phase) they collected a total of 248 arthropods, from flies from four families to millipedes and springtails. Only female and male Megaselia flies – M. scalaris and members of the M. angusta / longicostalis Clusters of closely related species, determined by DNA barcoding and morphology, have been found to have pollen in their flowers, indicating that they are the normal pollinators.

The authors then used gas chromatography with mass spectrometry (GC / MS) to analyze the bouquet of flowers. They found 16 compounds, including strong-smelling nitrogen- and sulfur-containing volatile molecules. The main ingredients included oligosulfides, produced by many species of plants whose pollinators are carrion flies or bats: a foul smell characteristic of the decomposition of meat. Surprisingly, another was 2,5-dimethylpyrazine (8-47% of total composition), a musty odor typical of cooked rice or roasted peanuts – which is known to be found in the shell of corrosive beetles and in the urine of rodents. Very few plants are known to produce this compound, which is strongly suggestive A. Microstom mimics an unusual bogus “reward” to attract specialized pollinators.

“Previous studies suggested this A. Microstom can be pollinated by leaf litter insects such as ants due to the orientation and position of the flowers. But here we show that this is incorrect: instead, it is the main pollinators Megaselia “Coffin flies”. As the name suggests, these flies feed on carrion on which they lay their eggs and which serves as food for the larvae, which is why they are often used as evidence in forensic medicine, ”says Dötterl.

“We show A. Microstom Flowers emit a simple but very unusual scent mixture that contains 2,5-dimethylpyrazine, a molecule that is not found in vertebrate carcasses or feces, but is found in dead beetles. We conclude from this A. Microstom likely uses a strategy never reported before: its flowers mimic the scent of invertebrate carrion to attract and contain pollinators. The special alignment of the flowers close to the ground can also be helpful, as pollinating coffin flies search for breeding grounds or food close to the ground, in leaf litter or between rocks, ”concludes co-author Prof. Stefan Wanke from the TU Dresden.

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