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Another New Plant Pollination Strategy: Fooling Food-Stealing Flies

  • Pollination of several angiosperms is based on deceit. In such systems, the flowers advertise a reward that ultimately is not provided. We report on a previously unknown pollination/mimicry system discovered in deceptive Aristolochia rotunda (Aristolochiaceae).Pollinators were collected in the natural habitat and identified. Flower scent and the volatiles of insects (models) potentially mimicked were analyzed by chemical analytical techniques. Electrophysiological and behavioral tests on the pollinators identified the components that mediate the plant–pollinator interaction and revealed the model of the mimicry system.The main pollinators of A. rotunda were female Chloropidae. They are food thieves that feed on secretions of true bugs (Miridae) while these are eaten by arthropod predators. Freshly killed mirids and Aristolochia flowers released the same scent components that chloropids use to find their food sources. Aristolochia exploits these components to deceive their chloropid pollinators.Aristolochia and other trap flowers were believed to lure saprophilous flies and mimic brood sites of pollinators. We demonstrate for A. rotunda, and hypothesize for other deceptive angiosperms, the evolution of a different, kleptomyiophilous pollination strategy. It involves scent mimicry and the exploitation of kleptoparasitic flies as pollinators. Our findings suggest a reconsideration of plants assumed to show sapromyiophilous pollination.
  • Pollination of several angiosperms is based on deceit. In such systems, the flowers advertise a reward that ultimately is not provided. We report on a previously unknown pollination/mimicry system discovered in deceptive Aristolochia rotunda (Aristolochiaceae).
  • Pollinators were collected in the natural habitat and identified. Flower scent and the volatiles of insects (models) potentially mimicked were analyzed by chemical analytical techniques. Electrophysiological and behavioral tests on the pollinators identified the components that mediate the plant–pollinator interaction and revealed the model of the mimicry system.
  • The main pollinators of A. rotunda were female Chloropidae. They are food thieves that feed on secretions of true bugs (Miridae) while these are eaten by arthropod predators. Freshly killed mirids and Aristolochia flowers released the same scent components that chloropids use to find their food sources. Aristolochia exploits these components to deceive their chloropid pollinators.
  • Aristolochia and other trap flowers were believed to lure saprophilous flies and mimic brood sites of pollinators. We demonstrate for A. rotunda, and hypothesize for other deceptive angiosperms, the evolution of a different, kleptomyiophilous pollination strategy. It involves scent mimicry and the exploitation of kleptoparasitic flies as pollinators. Our findings suggest a reconsideration of plants assumed to show sapromyiophilous pollination.
  • Actors involved in the newly discovered mimicry system and bioassay setup. (a) Flower of Aristolochia rotunda with a Trachysiphonella ruficeps individual at the margin of the flower tube. (b) Magnification of panel (a). (c) T. ruficeps pollinator collected from an A. rotunda flower in the female stage, carrying Aristolochia pollen on the head and thorax. (d) Flytrap used for bioassays. (e) T. ruficeps pollinator sticking to insect glue of a trap loaded with Mix ‘Aristolochia-Miridae’. (f) T. ruficeps individuals on a freshly killed Capsus ater. The fly in the upper part of the picture is feeding on C. ater secretions.
  • Aristolochia rotunda flower scent components are physiologically active in Trachysiphonella ruficeps. The black track represents the flower scent chromatogram (FID) of A. rotunda, and the gray track the respective electroantennogram (EAD) of T. ruficeps. Twenty-six components (see Table 1) consistently elicited a response in the antennae of female flies used for the measurements, of which the ones that elicited the strongest responses are indicated: 1, undecane; 2, hexyl butyrate; 3, (E)-2-hexenyl butyrate; 4, hexyl 2-methylbutyrate; 5, tridecane; 6, hexyl hexanoate; 7, (E)-2-hexenyl hexanoate + octyl butyrate; 8, decyl acetate; 9, unknown aliphatic hydrocarbon; 10, pentadecane; 11, unknown aliphatic; 12, decyl butyrate.
  • Behavioral response of pollinators to synthetic volatile mixtures and freshly killed true bugs. Two-choice bioassays (n, number of replicates) performed in the field testing a bait (synthetic mixtures or freshly killed true bugs) against a negative control (acetone for synthetic scent mixtures and the blank trapping devices for heteropterans). In all bioassays, there was no response to a negative control. The main pollinator of Aristolochia rotunda, Trachysiphonella ruficeps, only responded to synthetic mixtures and Miridae spp. but not to individuals of the other heteropteran families. The sex ratios of the flies are given in Tables S5 and S6. Exact binomial tests were performed (scent vs control) when applicable: ***, P ≤ 0.001; nt, not tested, owing to the small number of attracted flies.

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