Four to six percent of plants, distributed over different angiosperm families, entice pollinators by deception [1]. In these systems, chemical mimicry is often used as an efficient way to exploit the olfactory preferences of animals for the purpose of attracting them as pollinators [2,3]. Here, we report a very specific type of chemical mimicry of a food source. Ceropegia sandersonii (Apocynaceae), a deceptive South African plant with pitfall flowers, mimics attacked honeybees. We identified kleptoparasitic Desmometopa flies (Milichiidae) as the main pollinators of C. sandersonii. These flies are well known to feed on honeybees that are eaten by spiders, which we thus predicted as the model chemically mimicked by the plant. Indeed, we found that the floral scent of C. sandersonii is comparable to volatiles released from honeybees when under simulated attack. Moreover, many of these shared compounds elicited physiological responses in antennae of pollinating Desmometopa flies. A mixture of four compounds-geraniol, 2-heptanone, 2-nonanol, and (E)-2-octen-1-yl acetate-was highly attractive to the flies. We conclude that C. sandersonii is specialized on kleptoparasitic fly pollinators by deploying volatiles linked to the flies' food source, i.e., attacked and/or freshly killed honeybees. The blend of compounds emitted by C. sandersonii is unusual among flowering plants and lures kleptoparasitic flies into the trap flowers. This study describes a new example of how a plant can achieve pollination through chemical mimicry of the food sources of adult carnivorous animals.
Ceropegia species (Apocynaceae) have deceptive pitfall flowers and exploit small flies as pollinators, supposedly by chemical mimicry. Only preliminary data on the composition of flower scents are available for a single species so far, and the mimicry system is not yet understood in any species. We collected data on basic pollination aspects of C. dolichophylla, analyzed floral scent by gas chromatography linked to mass spectrometry (GC/MS), identified electrophysiologically active scent components by gas chromatography coupled with electroantennographic detection (GC/EAD), and determined compounds responsible for pollinator attraction in bioassays. We found that flowers of C. dolichophylla are visited by small flies of several taxa. Only Milichiidae and Chloropidae carried pollinaria and are, thus, pollinators. The pollen transfer efficiency (PTE) at two different sites was 2% and 4%, respectively. The floral scent was dominated by spiroacetals, mainly (2S,6R,8S)-8-methyl-2-propyl-1,7-dioxaspiro[5.5]undecane, n-tridecane, and N-(3-methylbutyl)acetamide. This spiroacetal and the acetamide elicited the most intense electrophysiological responses in fly antennae, and bioassays confirmed the capability of the spiroacetal in eliciting behavioral responses in pollinators. Most flies, determined as pollinators of C. dolichophylla, are kleptoparasites. They exploit insect prey of predatory arthropods as food source to which they are attracted by volatiles. undecane and N-(3-methylbutyl)acetamide have not been identified before as volatiles of other plants, however, they are known as insect volatiles. Both compounds occur in the venom glands of paper wasps, a potential food source for the pollinators of C. dolichophylla. We propose that C. dolichophylla shows a kleptomyiophilous pollination strategy. It mimics insect related odors to exploit the food-seeking behavior of its kleptoparasitic pollinators.
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