A systematic review suggests extension and redefinition of a food-deception pollination syndrome involving anautogenous flies.

Abstract

Background and aims: The currently recognized diversity of pollination strategies requires pollination syndromes to be updated. Described a decade ago, kleptomyiophily is a deceptive pollination system in which plants exploit the nutrient-seeking behavior of females of kleptoparasitic flies (Chloropidae and Milichiidae) by olfactorily mimicking their insect host. Such a pollination system was already hypothesized for pollination by biting midges (Ceratopogonidae) but has never been formalized. This review aims to explore the extent of pollination interactions deceiving anautogenous flies, especially by considering pollination by biting midges and kleptomyiophily as two facets of a common pollination syndrome: insect-host mimicry. As attraction of these flies seems to rely on insect-mimicking volatile organic compounds (VOCs), we propose an overview of the floral odours emitted by these plant species.

Methods: We compiled bibliographic data on plant species pollinated by Chloropidae, Ceratopogonidae and Milichiidae, to list plant species that could be involved in insect-host mimicry pollination strategies. Then, we reanalyzed data from the literature on floral VOCs of 18 of these plant species distributed among four plant families and compared them with related plant species performing brood-site mimicry, the pollination syndrome closest to insect-host mimicry.

Results: We show that at least 97 plant species from seven families are mainly pollinated by Chloropidae, Ceratopogonidae and Milichiidae, with almost exclusively females found in flowers. Deception of anautogenous flies has been shown for only four plant species but has been supposed for a total of 28 others. Comparison of floral VOCs shows significant differences between insect-host mimicry and brood-site mimicry in terms of chemical composition, diversity and models mimicked.

Conclusions: Despite fragmentary knowledge about the biology of the Diptera involved in insect-host mimicry, our results show similarities in floral odours and the putative mimicked resource between kleptomyiophilous plants and those pollinated by biting-midges, emphasizing a broader, unique, pollination syndrome.