Effective pollinia transfer by settling moths’ legs in an orchid Habenaria aitchisonii

Abstract

A great diversity of flower morphology in orchids has long been thought to be selected by diverse pollinators. Habenaria Willd. (Orchidaceae) species are generally characterized by long nectar spurs and pollinated by long‐tongued insects (Lepidoptera), the mechanical fit between the spur and pollinator proboscis length being supposedly caused by “arms race” reciprocal selection. Here, we report that flowers of Habenaria aitchisonii Rchb. f. with nectar spurs (approximately 9 mm) were pollinated by three species of settling noctuid moths whose proboscises varied in length from 10 to 16 mm. When a settling moth crawled on the spikes and probed the flowers for nectar, pollinia were placed on the moths’ legs rather than on other body parts. Our 5‐year survey of pollinia movement and 3‐year supplemental pollination experiments indicated that fruit and seed production in this orchid were not often pollen‐limited at flower level. In a natural population in Shangri‐La, Southwest China, the proportions of pollinia removal and deposition on stigmas by moth legs were 93.8% and 83.5%, respectively. This finding of efficient pollen transfer by the pollinators’ legs in H. aitchisonii adds a new example of diverse pollinia placement on pollinators (here settling moths) in the Orchidaceae.

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

“…Fruit set in our population of H. rhodocheila was relatively high and similar to other field studies of species in this genus including H. hieronymi (Singer & Cocucci, 1997), H. fordii (Zhang & Gao, 2017), and H. aitchisonii (Xiong et al., 2019). However, very low fruit set is also known in Habenaria (Ikeuchi et al., 2015; Singer & Cocucci, 1997; Thien & Utech, 1970).…”

“…In addition, the spur length of H. rhodocheila was longer than the proboscides of both butterfly species forcing the pollinators to ram their heads against the column to reach rewards deep in the spur. This is indicative of pollination by long‐tongued Lepidoptera in general (Micheneau et al., 2014 ) and common in other Habenaria species (Pedron et al., 2012; Singer & Cocucci, 1997; Tao et al., 2018; Xiong et al., 2019; Zhang & Gao, 2017). Pollinium attachment between the palpi of butterflies also occurred in the genus Bonatea s.l .…”

“…Furthermore, most Habenaria species also showed a similar high level of fruit set in populations with residential pollinators (Pedron et al, 2012;Singer et al, 2007;Xiong et al, 2019). Only a few species showed less than a 60% rate of natural fruit set (Thien & Utech, 1970;Xiong et al, 2015).…”

“…Worldwide field studies conducted in South America and Africa tend to predominate. Although 54 species are distributed in China (Chen & Cribb, 2009), Habenaria pollination has been reported in only six species in Yunnan province indicating that hawkmoths and/or other nocturnal moths were pollinators (Tao et al, 2018;Xiong et al, 2015Xiong et al, , 2019Zhang & Gao, 2017). No butterfly or other diurnal pollinators has been reported as Habenaria pollinators in China to date.…”

“…The pollinia of Habenaria species are usually attached to smooth body parts especially eyes (Moreira et al., 1996; Singer & Cocucci, 1997; Thien, 1969) and the bases of the proboscides (Singer, 2001; Xiong et al., 2015). To a lesser extent, the pollinia may be deposited on legs (Peter et al., 2009a; Xiong et al., 2019), thoraxes (Johnson et al., 2020; Sakagami & Sugiura, 2019), or on bare areas of the head (Suetsugu & Tanaka, 2014), or between the palpi (Pedron et al., 2012). Worldwide field studies conducted in South America and Africa tend to predominate.…”