Doing the twist: A test of Darwin's cross-pollination hypothesis for pollinarium reconfiguration

Abstract

Mating success in plants depends largely on the efficiency of pollen dispersal. For hermaphrodite plants, self-pollination, either within or among flowers, can reduce mating opportunities because of pollen and ovule discounting and inbreeding depression. Self-pollination may be particularly detrimental in plants such as orchids and asclepiads that package each flower's pollen into one or more pollinia which, together with accessory structures, comprise a pollinarium. Darwin proposed that physical reconfiguration of pollinaria serves as a mechanism for reducing the likelihood of self-pollination. To be effective, the time taken for pollinarium reconfiguration would need to exceed that spent by a pollinator on a plant. We investigated pollinarium reconfiguration (including pollinarium bending, pollinium shrinking and anther cap retention) in 19 species and found a strong positive relationship between reconfiguration time and the duration of pollinator visits. Reconfiguration times were also consistently longer than pollinator visit times. These results provide strong support for Darwin's idea that this mechanism promotes cross-pollination.

Figure 1

Pollinarium bending—the most common form of pollinarium reconfiguration. (a) A pollinarium of the orchid Eulophia parviflora freshly affixed to a cetoniid beetle will bend in the direction of the yellow arrow as indicated in (b) with the pollinarium half bent. (c) After ca 100 s the pollinarium has reconfigured and the paired pollinia can be inserted into the stigma (white arrow) as the beetle backs out of a flower in the direction of the white arrow (shown in cross-section). Scale bar, 5 mm.

Figure 2

(a) There is a positive relationship between pollinarium reconfiguration and pollinator visit times. The data points are above the dashed line of unity, indicating that pollinarium reconfiguration tends to take place after the end of a pollinator visit. (b) The positive relationship between phylogentically independent contrasts of pollinarium reconfiguration and pollinator visit times.