The lady’s ‘slippery’ orchid: functions of the floral trap and aphid mimicry in a hoverfly-pollinated Phragmipedium species in Brazil

Abstract

Background and Aims Trap flowers are fascinating cases of adaptation, often linked to oviposition site mimicry systems. Some trap flowers do not imprison pollinators for a pre-determined period, but rather force them to move through a specific path, manipulating their movements in a way that culminates in pollen transfer, often as they leave through a secondary opening. Methods We investigated the previously unknown pollination system of the lady’s slipper orchid Phragmipedium vittatum and assessed the function of micro-morphological traits of its trap flowers. Key Results Our observations revealed that P. vittatum is pollinated by females of two hoverfly species (Syrphidae). Eggs laid by flies on or near raised black spots on the flowers indicate that the orchid mimics aphids which serve as food for their aphidophagous larvae. Dark elevated aphid-like spots appear to attract the attention of hoverflies to a slipping zone. This region has downward projecting papillate cells and mucilage secretion that promote slipperiness, causing potential pollinators to fall into the labellum. They then follow a specific upward route towards inner aphid-like spots by holding onto upward oriented hairs that aid their grip. As hoverflies are funneled by the lateral constriction of the labellum, they pass the stigma, depositing pollen they may be carrying. Later, they squeeze under one of the articulated anthers which places pollen smears onto their upper thorax. Then, they depart through one of the narrow lateral holes by holding onto hairs projecting from the petals. Conclusions This study confirms the system of aphid mimicry in Phragmipedium and highlights the sophisticated micro-morphological traits used by trap flowers in pollinator attraction, trapping, guidance, and release, thus promoting precise pollen transfer.

Incomplete resupination during floral development leads to pollination failure in a slipper orchid

“…Although the proportion of flowers with incomplete resupination was lower than those with normal orientation, this may still reduce the overall reproductive output of the population. Since P. vittatum is incapable of autonomous self-pollination (Cardoso et al 2023), the ~10% with incomplete resupination will fail to reproduce. This is important since the orchid species is pollen-limited, with a mean of 16.1% of flowers receiving pollen over a sampling period of 4 years (Cardoso et al 2023).…”

“…Since P. vittatum is incapable of autonomous self-pollination (Cardoso et al 2023), the ~10% with incomplete resupination will fail to reproduce. This is important since the orchid species is pollen-limited, with a mean of 16.1% of flowers receiving pollen over a sampling period of 4 years (Cardoso et al 2023). These results indicate that flowers do not reach their maximum reproductive potential.…”

“…These results indicate that flowers do not reach their maximum reproductive potential. Since a single fruit can bear more than 100,000 seeds (Cardoso et al 2023), the reduction in fruit set due to ontogenetic errors can compromise population viability of P. vittatum, which is a threatened species present in environments highly impacted by human activity, such as soil drainage and farming (Gonc ßalves et al 2022). Several genetic (e.g., mutation, hybridization, homozygosity, genetic individual differences) and environmental (e.g., herbivory, competition, radioactive and ultraviolet radiation, artificial fertilizers, pollutants, extreme saline conditions) factors may cause developmental stress and impair the pollination process (Møller & Shykoff 1999;Møller 2000).…”

“…During 8 days in 2021, newly opened resupinate flowers from previously bagged buds were submitted to one of the following treatments: (1) non-resupination: flowers were tied on the bracts in an upside-down position, with the labellum uppermost (%0°; n = 17); (2) half-resupination: flowers were tied in a lateral position with the labellum facing sideward (%90°; n = 31); (3) full resupination: flowers were tied in their normal position with the labellum downmost (%180°; n = 35); and (4) control: flowers were only unbagged without the placement of the wire (%180°; n = 28). Male and female pollination performance (i.e., pollen smear removal and deposition, respectively; sensu Arnold 1983; Opedal 2021) were checked on day 5 after treatment by visually inspecting the absence of pollen on anthers and presence on stigmas, respectively (sensu Cardoso et al 2023).…”

“…Male and female pollination performance ( i.e ., pollen smear removal and deposition, respectively; sensu Arnold 1983; Opedal 2021) were checked on day 5 after treatment by visually inspecting the absence of pollen on anthers and presence on stigmas, respectively ( sensu Cardoso et al . 2023).…”