Why two kinds of stamens in buzz-pollinated flowers? Experimental support for Darwin's division-of-labour hypothesis

Summary

• 1
  Most animal-pollinated flowering plants offer nectar as a reward for their pollinators. Some 20 000 species, however, offer only pollen and rely on pollen-foraging bees for pollination. This creates a dilemma since pollen grains contain the male gametes and should be protected from becoming bee food. Darwin was the first to hypothesize that a ‘division-of-labour’ among stamens could solve this dilemma, with some stamens providing pollen as food, others providing pollen for fertilization. This hypothesis can only be tested if pollen grains from the two sets of stamens can be distinguished and their fates determined to the point of attachment on the stigma.
• 2
  We tested Darwin's hypothesis in Melastoma malabathricum (Melastomataceae), a pollen-only flower with conspicuously differentiated stamens, an inner set that is short and yellow and an outer set that is much longer and purple with small yellow spurs. Pollen release is through terminal anther pores. Taking advantage of different exine patterns on the pollen produced by the two sets of stamens, we carried out a series of experimental manipulations to compare pollinator foraging behaviour and pollen pathways from anthers to stigmas.
• 3
  The results demonstrate that in spite of all 10 stamens being buzzed simultaneously by the carpenter bees that pollinate M. malabathricum, pollen from the purple ‘fertilization’ stamens is dramatically more likely to land on stigmas than pollen from the yellow ‘feeding’ stamens. Removal experiments showed that the yellow ‘feeding’ stamens also attracted pollinators from a distance. Flowers that had their anther pores plugged received fewer buzzing bouts per visit, indicating that bees assessed the amount of pollen received per bout. Surprisingly, there was no significant difference in pollen loads on stigmas of flowers that had their anthers plugged and stigmas of controls, demonstrating the efficiency of vector-assisted cross-pollination and the lack of vector-assisted self-pollination.
• 4
  The unexpectedly precise placement of pollen grains even with buzz pollination, with a large proportion of the grains deposited out of the bees’ grooming reach, helps explain the evolutionary persistence of pollen as a reward in spite of the bees’ ability to assess the amount of pollen received during foraging bouts. Together, these results strongly support Darwin's division-of-labour hypothesis.