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The pollination of Habenaria rhodocheila (Orchidaceae) in South China: When butterflies take sides.

ABSTRACT: Habenaria is one of the largest terrestrial genera in the family Orchidaceae. Most field studies on Habenaria species with greenish-white and nocturnal scented flowers are pollinated by nocturnal hawkmoths and settling moths. However, H. rhodocheila presents reddish flowers lacking a detectable scent and fails to fit the moth pollination syndrome. We investigated the pollinators, breeding system, and functional traits of H. rhodocheila in South China and found that two diurnal swallowtail butterflies Papilio helenus and Papilio nephelus (Papilionidae) were the effective pollinators. When butterflies foraged for nectar in the spur, the pollinia became attached between the palpi. A triangular projected median rostellar lobe was found at the entrance (sinus) of the spur of H. rhodocheila. This lobe divided the spur opening into two entrances forcing butterflies to enter their proboscides through the left or right side. When the projection of median rostellar lobe was removed, the site of pollinium attachment changed to the eyes of the butterflies, leading to a higher rate of pollinium removal but lower rate of pollinium deposition. Our quartz glass cylinder choice experiment suggested that visual rather than olfactory cues provided the major stimuli for butterflies to locate these flowers. Hand pollination experiments suggested this species was self-compatible but pollinator-dependent. However, the proportion of seeds with large embryos produced in self-pollinated fruits was significantly lower than in cross-pollinated fruits, indicating a significant inbreeding depression. Unlike many other orchid species, fruit set was higher than rates of pollinium removal, indicating a high level of pollination efficiency in a species with friable pollinia. Shifts from moth to butterfly pollination in the genus Habenaria parallel other orchid lineages providing insights into the potential for pollinator-mediated floral trait selection.

SUBMITTER: Chen XH

PROVIDER: S-EPMC7981216 | biostudies-literature | 2021 Mar

REPOSITORIES: biostudies-literature

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The pollination of Habenaria rhodocheila (Orchidaceae) in South China: When butterflies take sides.

Chen Xing-Hui XH Tan Shao-Lin SL Liang Yue-Long YL Huang Lang L Xiao Han-Wen HW Luo Huo-Lin HL Xiong Dong-Jin DJ Yang Bo-Yun BY Ren Zong-Xin ZX

Ecology and evolution 20210302 6

Habenaria is one of the largest terrestrial genera in the family Orchidaceae. Most field studies on Habenaria species with greenish-white and nocturnal scented flowers are pollinated by nocturnal hawkmoths and settling moths. However, H. rhodocheila presents reddish flowers lacking a detectable scent and fails to fit the moth pollination syndrome. We investigated the pollinators, breeding system, and functional traits of H. rhodocheila in South China and found that tw ...[more]

PMID: 33767841

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Project description:Background and aimsLepanthes is one of the largest angiosperm genera (>800 species). Their non-rewarding, tiny and colourful flowers are structurally complex. Their pollination mechanism has hitherto remained unknown, but has been subject of ample speculation; the function of the minuscule labellum appendix is especially puzzling. Here, the pollination of L. glicensteinii by sexually deceived male fungus gnats is described and illustrated.MethodsVisitors to flowers of L. glicensteinii were photographed and their behaviour documented; some were captured for identification. Occasional visits to flowers of L. helleri, L. stenorhyncha and L. turialvae were also observed. Structural features of flowers and pollinators were studied with SEM.Key resultsSexually aroused males of the fungus gnat Bradysia floribunda (Diptera: Sciaridae) were the only visitors and pollinators of L. glicensteinii. The initial long-distance attractant seems to be olfactory. Upon finding a flower, the fly curls his abdomen under the labellum and grabs the appendix with his genitalic claspers, then dismounts the flower and turns around to face away from it. The pollinarium attaches to his abdomen during this pivoting manoeuvre. Pollinia are deposited on the stigma during a subsequent flower visit. The flies appear to ejaculate during pseudocopulation. The visitors of L. helleri, L. stenorhyncha and L. turialvae are different species of fungus gnats that display a similar behaviour.ConclusionsLepanthes glicensteinii has genitalic pseudocopulatory pollination, the first case reported outside of the Australian orchid genus Cryptostylis. Since most species of Lepanthes have the same unusual flower structure, it is predicted that pollination by sexual deception is prevalent in the genus. Several morphological and phenological traits in Lepanthes seem well suited for exploiting male fungus gnats as pollinators. Correspondingly, some demographic trends common in Lepanthes are consistent with patterns of male sciarid behaviour.

Dataset Information

The pollination of Habenaria rhodocheila (Orchidaceae) in South China: When butterflies take sides.

Publications

The pollination of <i>Habenaria rhodocheila</i> (Orchidaceae) in South China: When butterflies take sides.

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