Athayde Tonhasca Júnior has returned with his patented text-and-photo piece on (you guess it) pollination. Athayde’s captions and IDs are indented, and you can enlarge his photos by clicking on them.
Delicate trade agreements
In one of the regular letters to his close friend, explorer and botanist Joseph Hooker, Charles Darwin vented his frustration at a puzzle he hadn’t been able to crack: …I will return the 3 Melastomateds; I do not want them & indeed have cuttings; I am very low about them, & have wasted enormous labour over them & cannot yet get a glimpse of the meaning of the parts. (Darwin, 1862). The ‘Melastomateds’ cuttings belonged to the family Melastomataceae, a huge group (some 5,000 known species) of mostly tropical shrubs, trees, herbs and lianas. The ‘parts’ whose meaning eluded Darwin were the stamens and anthers.
A complete, hermaphroditic flower. The pistil comprises the ovary, the style (a pillar-like stalk through which pollen germinates to reach the ovary) and the stigma (a sticky tip at the top of the style that receives pollen). The stamen has a filament that supports the anther, where pollen is produced © Anjubaba, Wikimedia Commons:
For a range of Melastomataceae species and at least 15 other flowering plant families, there are two (sometimes three) types of morphologically distinct stamens and anthers in each flower, a condition known as heteranthery. Typically, one set comprises short, colourful stamens located at the centre of the flower. The other set has longer, less colourful stamens that are deflected to the flower’s side and curved inwards. Darwin wrote a whole book about flower morphologies and their bearings in natural selection (Darwin, 1877), but the relevance – if any – of heteranthery puzzled him. He suspected the condition was related to reproduction, but he couldn’t figure out how.
An Asian melastoma (Melastoma candidum) flower with shorter stamens/yellow anthers, and longer stamens/reddish anthers © Hachiman et al., 2024:
Darwin got his answer from his correspondent and enthusiastic evolutionist Fritz Müller (1822- 1897) working in faraway southern Brazil. Müller, a Prussian immigrant, was a brilliant naturalist who wrote about biology, morphology, systematics and evolution of plants, marine invertebrates, butterflies, ants, termites and other insects. Müller discovered the nutritious bodies (today called Müllerian bodies), which are plant glands that secrete ant food, and demonstrated that pairs of poisonous, unpalatable species benefit from evolving a similar appearance to reduce their chances of being attacked, a form of protection we know as Müllerian mimicry.
Fritz Müller kitted out to go exploring a Brazilian tropical forest © O Município;
From his observations of Melastomataceae, Fritz Müller and his botanist brother Hermann – who stayed in Prussia – proposed that the two types of stamen played different roles. One type was specialised in transferring pollen to flower visitors; the other was responsible for feeding them. But why would a plant come to such an elaborate ruse?
Most Melastomataceae and many heterantherous species are pollinated by bees, but their flowers don’t produce any nectar: pollen is their sole food reward. This creates a dilemma. Plants must hand out pollen, otherwise bees wouldn’t pay a visit. But the giveaway must be sparing, otherwise reproduction could be curtailed or prevented altogether. Heterantherous plants sorted this problem by dividing up pollen allocation. The showy, central stamens attract bees, who store the collected pollen in their pollen baskets (scopa): this pollen is no longer available for fertilisation. The longer stamens that curve away from the centre are in a convenient position to sneak on a foraging bee and deposit pollen on parts of her body from where they are not easily scooped up by grooming. With luck, these pollen grains will be transported to another plant’s stigma.
Xylocopa flavifrons (A) and Amegilla urens (B) collecting pollen from Melastoma malabathricum‘s feeding stamens (yellow) and being exposed to pollinating stamens (red). Arrows indicate the pollen-receiving stigmas © Hachiman et al., 2024:
The Müller brothers’ ‘division of labour hypothesis’, as it is known today, was a revelation to Darwin: I have had a letter from Fritz Müller suggesting a novel and very curious explanation of certain plants producing two sets of anthers of different colour. This has set me on fire to renew the laborious experiments which I made on this subject, now 20 years ago (Darwin, 1887).
Division of labour is beautifully exemplified by the pollination of Rhynchanthera grandiflora, a shrub native to the Neotropical region. This plant has flowers with four short stamens and one long stamen, all of them with upwards-facing anthers. A bee lands on a flower, grabs the short stamens and starts flexing her thoracic muscles at high frequency, generating vibrations that are transmitted to the anthers. These moves, known as ‘buzz pollination’, release pollen that lands on the bee. This tricky form of pollen extraction is restricted to some specialised bees such as bumble bees (Bombus spp.) and carpenter bees (Xylocopa spp.). Pollen released from anthers in the short stamens is scooped up by the bee. Pollen from the anther on the long stamen shoots up and sticks to the bee’s dorsal side (Konzmann et al., 2020).
L: A R. grandiflora flower. R: A bumble bee buzz-pollinating depresses the long stamen with its abdomen. The dotted line and cone show the mean direction and scattering angle, respectively, of the released pollen © Konzmann et al., 2020:
The division of labour hypothesis has been confirmed for a few other heterantherous, bee-pollinated species. But, as is invariably the case in biology, things are a bit more complicated.
The hypothesis requires that both types of stamens produce pollen at the same time. But that’s not the case for speckled clarkia (Clarkia cylindrica) and elegant clarkia (C. unguiculata), both natives to western North America. These plants have two types of stamens that mature gradually and at different times. Moreover, pollen from both types of stamens is collected for food and transferred between flowers in equal proportions, so there’s no indication of labour division. For Kay et al. (2020), heteranthery in Clarkia spp. and possibly other heterantherous plants is a mechanism to dispense pollen gradually, during several visits by bees. This strategy would enhance pollination because a bee with only a few pollen grains attached to her body is likely to move to another flower without wasting time grooming herself to remove pollen from her body. Why then bother with two types of stamens? Different morphologies and development times represent additional insurance against excessive pollen harvesting.
A speckled clarkia is a miserly pollen-giver © U.S. National Park Service, Wikimedia Commons:
We don’t have enough studies to assess the relative significance of the division-of-labour hypothesis or the pollen-dosing strategy. Either way, dividing up the pollen stock or releasing it slowly are tactics to give away as little as possible a metabolically expensive product without discouraging flower visitors, who aim to gather as much of it and as fast as possible. The morphological adaptations exhibited by heterantherous plants are examples of the true nature of plant-pollinator interactions: an equilibrium between two parties with conflicting interests fine-tuned by natural selection.
References
Darwin, C.R. 1862. Letter no. 3762, Darwin Correspondence Project, https://www.darwinproject.ac.uk/.
Darwin, C.R. 1877. The Different Forms of Flowers on Plants of the Same Species. John Murray.
Darwin, F. (ed). 1887. The Life and Letters of Charles Darwin, Including an Autobiographical Chapter. John Murray.
Hachiman, S. et al. 2024. Division of labour between dimorphic stamens in Melastoma candidum (Melastomataceae): Role of stamen strength in the biomechanics of pollination. Journal of Pollination Ecology 37: 284–302.
Kay, K.M. et al. 2020. Darwin’s vexing contrivance: a new hypothesis for why some flowers have two kinds of anther. Proceedings of the Royal Society B 287: 20202593.
Konzmann, S. et al. 2020. Morphological specialization of heterantherous Rhynchanthera grandiflora (Melastomataceae) accommodates pollinator diversity. Plant Biology 22: 583-590.
Fantastic how the plants outsmart the bees—all mediated by natural selection, of course. When was it first discovered how pistils and stamens function in plant reproduction? My guess is that anecdotal knowledge is thousands of years old, but what about the modern scientific understanding?
I really enjoy these posts!
The depth of the subject of plant-insect interactions never ceases to amaze.
Thank you for sharing!
Very interesting. Thanks.
Cool plant photos and information, thanks!
Thanks once again for these informative and entertaining posts.
Interesting post on a pollination strategy. But while it may work on larger bees like genus Xylocopa, smaller bees, like the Small Carpenter Bees (genus Ceratina) can collect pollen from the longer stamens directly.
Here’s an example: my iNaturalist observation of a Small Carpenter Bee gathering pollen from a Melastoma malabathricum [ https://www.inaturalist.org/observations/119202536 ].
Fascinating, as always – thanks!