Flies can be pollen thieves but plants deal with them

Pollinators usually have good PR. In the last couple of decades, insect pollinator populations have been declining, causing havoc in ecosystems and for food production. Insect-pollinated plants can maintain higher genetic diversity as the pollinators carry pollen from (likely) the same species, enabling cross-fertilisation across long distances. In return for a visit, the insects can consume or collect some pollen from the plants. 

Sometimes, pollinators can be greedy or wasteful and take more pollen from a plant than they effectively transfer to the next plant. Plants can experience pollen limitation if they do not have enough pollinators or do not receive enough pollen. This limitation leads to fewer seeds. 

Dr Alison Brody and Alexander Burnham from the University of Vermont, with Brittany Smith from the Rocky Mountain Biological Laboratory, investigated if flies are pollen thieves of the normally bumblebee-pollinated towering Jacob’s-ladder (Polemonium foliosissimum) plant in Colorado (USA) and how pollination limitation impacts the populations. 

In the latest study published in Annals of Botany, the researchers hypothesised that if flies (muscids) are pollen thieves, the female P. foliosissimum plants would be more pollen limited and so produce fewer seeds overall compared to the hermaphrodites. Brody and colleagues suggest that pollen limitation is caused by the lack of effective pollinators (bumblebees) rather than the lack of pollen for P. foliosissimum.

Back in 2015, Clarke and Brody surveyed 28 populations around the Elk Mountains in Colorado and found that almost all plants were gynodioecious (hermaphrodite or function only as females). In another study, Clarke and Brody investigated why it might be advantageous for sticky polemoniums to have female plants alongside hermaphrodites – a question that Darwin himself asked centuries ago. Losing the male function (producing pollen) might conserve some resources and enable plants to invest more in seed production. However, female plants rely entirely on pollinators for reproduction. 

In 2015, Brody and colleagues made detailed observations of pollinators on P. foliosissimum plants around subalpine meadows over two years. The research team collected the stigmas to count conspecific and other pollen grains under the microscope and quantified the pollen from dried anthers. This count allowed the team to quantify how much pollen was deposited by each visitor. 

Next, the researchers manipulated the ratio of hermaphrodites and female plants and removed half of the anthers of some plants to investigate the presence – and effect – of pollen limitation. In the second year of the experiments, the scientists also hand-pollinated plants to “undo” pollination limitation and compared seed production between pollen-removed and hand-pollinated treatments. 

Flies were the most frequent visitors and deposited less pollen than bumblebees in a single visit. In the first year, plants received 28-32% less pollen when the anthers were removed in the neighbourhood. There was no significant pollen reduction in the second year. Hand-pollination increased the number of seeds for both hermaphrodites and females, and overall, female plants produced the most seeds. 

“We expected that pollen reduction by muscid flies, or experimentally, would exacerbate pollen limitation for P. foliosissimum at our study site,” Brody and colleagues write. 

“[A]lthough both sexes were pollen limited as demonstrated by a significant increase in seeds/fruit when hand pollinated and a marginally significant increase in fruit set, plants were no more pollen limited in neighborhoods where pollen had been reduced than in control neighborhoods […].” The authors conclude, “Thus, for P. foliosissimum, pollen limitation is caused by a lack of effective pollinators as formerly concluded rather than a lack of pollen per se.”

Wind-pollinated and self-compatible plants have different mechanisms around relying on pollinators but are threatened by low genetic diversity. Insect-pollinated plants will be in real trouble if pollinator populations continue to decline in the future. 

“[S]everal bumblebees as well as many other insects are experiencing global declines. As the absolute and relative abundance of legitimate and illegitimate pollinators change, we may expect pollen theft to have larger effects,” Brody and colleagues warn. 

This study has identified flies as pollen thieves of the towering Jacob’s-ladder plant. The research team has shown how detailed observations and sex ratio and/or pollen availability manipulations can find the root of pollination limitation.