Sexually deceptive orchids with distinct flower morphologies elicit different behaviours from a shared pollinator

Pollination by sexual deception is one of the most specialized pollination strategies among angiosperms, with co-occurring plant species often exploiting males of different insect species. We test if the morphologically divergent orchids Caladenia cardiochila and its sympatric endangered congener C. lowanensis are dependent on the same thynnine wasp pollinator. We further investigate the role of floral traits on pollinator behaviour and evaluate potential hybridization risk.

Pollinator sharing was tested for with DNA barcoding. Pollinator behaviour was quantified and experimental floral dissections were used to determine the site of sexual attractant release. We employed GC-MS to test for the presence of sugar on orchid labella, hand crosses to assess the impact of interspecific pollen transfer on seed viability, and population monitoring to quantify natural pollination success.

We found that C. cardiochila and C. lowanensis both employ sexual deception of Phymatothynnus aff. nitidus wasps as a pollination strategy. However, the behaviour they elicit differs, with wasps attempting to mate with the insectiform labellum in C. cardiochila and the glandular sepal tips in C. lowanensis, which are the respective sources of sexual attractant. Unlike most sexually deceptive orchids, C. lowanensis secretes minute amounts of sugar from its labellum. While wasps interacted more frequently with the labellum in C. cardiochila, placing them closer to its reproductive structures, both species exhibited comparable pollination success and pollen transfer efficiency. Experimental crosses revealed that hybrid seed has high viability.

Sexual deception of the same pollinator by orchids varying in the location of sexual attractant and flower morphology highlights the considerable flexibility of this pollination strategy. Given their overlapping distributions and the viability of hybrid seed, pollinator sharing poses a hybridization risk that needs to be considered in the management of wild C. lowanensis populations and future conservation translocations.