Pollination by deceit in Paphiopedilum barbigerum (Orchidaceae): a staminode exploits the innate colour preferences of hoverflies (Syrphidae)

Abstract

Paphiopedilum barbigerum T. Tang et F. T. Wang, a slipper orchid native to southwest China and northern Vietnam, produces deceptive flowers that are self-compatible but incapable of mechanical self-pollination (autogamy). The flowers are visited by females of Allograpta javana and Episyrphus balteatus (Syrphidae) that disperse the orchid's massulate pollen onto the receptive stigmas. Measurements of insect bodies and floral architecture show that the physical dimensions of these two fly species correlate with the relative positions of the receptive stigma and dehiscent anthers of P. barbigerum. These hoverflies land on the slippery centralised wart located on the shiny yellow staminode and then fall backwards through the labellum entrance. They are temporarily trapped in the inflated chamber composed of the interconnected labellum and column. The attractive staminode of P. barbigerum strongly reflects the colour yellow (500-560 nm), a colour preferred innately by most pollen-eating members of the Syrphidae. No scent molecules were detected using GC mass spectrometry analysis, showing that the primary attractant in this system is visual, not olfactory. Pollination-by-deceit in P. barbigerum is contrasted with its congener, P. dianthum, a brood site mimic that is pollinated by ovipositing females of E. balteatus. As the natural rate of fruit set in P. barbigerum (mean 26.3% pooled over three seasons) is lower than that of P. dianthum (mean 58.5% over two seasons), the evolution of false brood sites in some Paphiopedilum spp. should be selectively advantageous as they may provide an increase in the attention and return rates of dependable pollinators to flowers that always lack a reward.

Trait evolution in the slipper orchidPaphiopedilum(Orchidaceae) in China

“…Flowers of these slipper orchids in China are thought to be pollinated by deceit, usually relying upon morphology and scent to attract pollinators. 11,12,18,19 Therefore, they may reduce their investment in flower color. Moreover, color as perceived by human observers is likely to be quite different than that perceived by pollinators.…”

“…13 However, ten species of Paphiopedilum are pollinated by hoverflies ( Table 2.). [10][11][12][22][23][24][25] The subglobose-shaped lip, with involute margins apically, may help prevent access by insects with larger bodies. Members of subgenus Paphiopedilum include P. parishii, P. dianthum, P. appletonianum, P. wardii, P. venustum, P. purpuratum, P. spicerianum, P. insigne, P. barbigerum, P. tranlienianum, P. tigrinum, P. charlesworthii, P. helenae, and P. villosum, all of which have helmet-shaped lips that have large, deep mouths but no involute margins.…”

“…7 Several studies have successfully demonstrated that variation in floral traits among groups is a consequence of adaptation to different pollinators. 7,11,12 However, another research has found no evidence that pollinator specialization has driven speciation in the Orchidaceae. 26 Staminode shape exhibits high morphological diversity within Paphiopedilum, playing an important role in species identification.…”

“…7,9 However, analyses of pollination ecology have been conducted for only a few species within that genus. [10][11][12] ) and phylogenetic studies on the evolution of their plant traits are scarce. 8 This shortcoming is probably not due to a lack of examples for trait diversity within genera or families, but rather because botanists tend to study single species in detail, without a comparative perspective.…”

“…Bees and hoverflies are the main pollinators of Chinese orchids and drive the diversification of Paphiopedilum (Banziger, 1996;Shi et al, 2006Shi et al, , 2009Liu et al 2009;Tang et al 2014). Most species of Paphiopedilum in China are reported as growing terrestrially or facultative eiphytically, fewer species are found to be lithophytes (P. villosum and P. parishii).…”