Hawkmoth pollination of the orchid Habenaria clavata: mechanical wing guides, floral scent and electroantennography

Abstract

Floral morphology can play a key role in mechanically guiding pollinators towards reproductive structures, particularly when visibility is limited at night, but the functional significance of morphological traits has seldom been considered in this context. Here we describe a remarkably intricate pollination mechanism in the hawkmoth-pollinated African grassland orchid Habenaria clavata, and also document aspects of the reproductive success and chemical ecology of this pollination system. The flowers are pollinated by several short-tongued hawkmoths, particularly Basiothia schenki, which was the most frequent visitor and occurred at all sites. Moths are probably attracted by the strong scent, which was dominated by several oxygenated aromatics that also elicited strong electrophysiological responses from antennae of B. schenki. Apart from the white rostellum lobes and stigma, which serve as a visual guide to the spur entrance, the flower parts are entirely green and indistinguishable from leaves in terms of spectral information. Using motion-activated video cameras we established that the leading edges of the forewings of foraging hawkmoths contact the two upwardly curving petal lobes, and that hawkmoths are then apparently mechanically guided down onto the reproductive structures. Pollinaria are attached in an unusual place – among hairs on the ventral surface of the thorax, between the middle legs – and are brushed over the protruding stigma lobes when the proboscis is fully inserted in the 41-mm-long spur. These results highlight how multiple traits (morphology, spectral reflectance and scent) can act synergistically to ensure transfer of pollen among flowers.

Food Reward Chemistry Explains a Novel Pollinator Shift and Vestigialization of Long Floral Spurs in an Orchid

“…To further explore the presence of floral oil-derived compounds, we analyzed pentane extracts of flowers by using gas chromatography coupled with mass spectrometry (GCMS), to identify the presence of diacetin. 8,36 This volatile acetylated glycerol is thought to be a derivative of the biosynthesis of fatty floral oil, and is considered a universal cue for oil-collecting bees, including R. neliana, the pollinator of the BEE form. 8 Consistent with the results from staining, GCMS analyses confirmed the presence of diacetin and also triacetin in all six forms ( Figure 2).…”

“…Several aromatic compounds in the S. longicauda headspace are known to elicit antennal responses in the hawkmoth pollinator B. schenki. 36 Given the overall similarity in flower shape, color, and headspace scent, we predicted that the lack of nocturnal moth visitation to the BEE form could reflect the lack of a suitable reward. Measurements of nectar volume and sugar concentration confirmed an almost complete absence of nectar in the floral spurs of the BEE form, whereas in the MOTH forms, nectar volume per flower ranged between 0.5-2.5 ml, resulting in a total sugar availability per flower of 0.2-0.8 mg ( Figure 2).…”

“…8 Presence of diacetin has been reported for another moth-pollinated orchid in a study that also found that moth antennae respond to it. 36 More research is needed to understand the presence of diacetin in species that are not bee pollinated, in order to clarify whether it is a legacy of ancestral pollination by oil-collecting bees or has a functional role in these species.…”

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

“…The importance of this key, floral trait was confirmed 135 years later (Alexandersson & Johnson, 2002; Balducci et al., 2019; Martins & Johnson, 2007; Nilsson, 1988; Wasserthal, 1997). However, the function of a spur matching a proboscis cannot be understood without the investigation of other signals and/or effective pollen transfer traits targeting pollinium attachment to the pollinator and receptive stigma lobes (Johnson et al., 2020; Pedron et al., 2012; Tao et al., 2018). Such studies remain uncommon (Johnson et al., 2020).…”

Different Morphs of Heterostylous Plant (Tirpitzia Sinensis) Associated With Floral Characters Have Various Adaptation Strategies to Pollinator to Ensure Reproductive Success

“…Hawkmoths are important pollinators found in some warm areas at dusk that y forward with a fast wing beat and feed from owers with exceptionally long tongues while hovering [16]. Hawkmoth pollination has been reported in a wide range of angiosperm taxa [17][18][19]. Tirpitzia sinensis (Linaceae) is an odourless distylous plant with white narrow tubular owers.…”