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Flowering plants came to dominate the landscape
The great explosion in flowering plants during the Cretaceous Period is one of the great enigmas of evolution.
Charles Darwin had no explanation, calling it an "abominable mystery".
But now scientists think they have solved the riddle of how flowers came to dominate the conifers and ferns that preceded them.
The flowers' secret, they say, was to exploit a change in soil fertility, and create a feedback loop that allowed new flowers to feed off dead ones.
The relative explosion of flowering plants greatly worried Darwin.
In a letter written on 8 March 1875 to palaeobotanist Oswald Heer, he said: "The sudden appearance of so many Dycotyledons in the Upper Chalk appears to me a most perplexing phenomenon to all who believe in any form of evolution."
In a later letter to botanist Joseph Hooker, head of the Royal Botanic Gardens at Kew, Darwin described it as an "abominable mystery".
The great problem for Darwin and others at that time was that the Late Cretaceous was very rich in fossil angiosperm (flowering plant) species, while the Early Cretaceous was almost devoid of any early examples.
This rapid bloom in flowering plant species did not fit Darwin's belief that evolution was an extremely gradual process.
Since then, many more fossils of flowering species have been discovered, showing that they emerged over a longer period.
Today scientists believe that at the start of the Cretaceous Period, 125 million years ago, gymnosperms, the group of plants that contains cycads and conifers, dominated the globe.
Just a few groups of angiosperms had evolved, and these were rather small fragile plants that probably grew in aquatic environments, or alongside streams.
The explosion of flowering life occurred over a 40 to 50 million year period
Some are also thought to have colonised extremely dry, possibly salty places, since they had quite thick leaves which would have helped conserve water.
But then, between 125 and 65 million years ago, these flowering plants exploded into life.
For example, around 105 million years ago between five and 20% of all plant species were angiosperms. By 65 million years ago, over 80% were flowering plants.
"The change from a gymnosperm- and fern-dominated world to a world dominated by fast-growing angiosperms is one of the most important changes in the history of the biosphere of our Earth, with enormous consequences for the opportunities of mammals," says Frank Berendse, an ecologist at Wageningen University in The Netherlands.
"Although the change in diversity occurred much more gradually than thought at Darwin's time, the change in abundance occurred very fast," Berendse says.
Berendse and Wageningen University colleague Marten Scheffer now think they can explain how it happened.
All shapes and colours
They outline their idea in the journal Ecology Letters.
Initially, gymnosperms flourished in poor soils. Such plants have longer-lived leaves which are capable of squeezing more nutrients out of the ground, but the litter they create tends not to decompose very fast. So while gymnosperms benefit from poor soils, they also do little to improve soil quality.
But then came some subtle changes in soil fertility. Angiosperms started colonising more fertile soils, gaining a foothold.
These early flowering plants then began changing the ecology of the soil. As they perished, they create a greater turnover in litter that replenished the soil, allowing yet more flowers to grow.
"From that time a positive feedback developed, where an increase in angiosperm dominance led to an increase in soil fertility and an increase in soil fertility led to a further accelerated expansion of the angiosperms," says Berendse.
The idea that such sudden shifts in vegetation can occur is supported by evidence from the modern day.
Over the past 30 years, heathlands in western Europe have gone from being dominated by dwarf shrubs to perennial grasses, the researchers say.
Ferns once ruled
Like gymnosperms, the shrubs have long-lived leaves and stems which minimise the loss of nutrients but prevent the plants growing fast.
But once the grasses took hold, their faster growth rates created a feedback loop which added more nutrients to the soil, allowing yet more grass to grow.
A similar shift has also taken place in raised bogs, in which peat mosses can quickly be out-competed by vascular plants, say the researchers.
Berendse's and Scheffer's idea remains a hypothesis for now.
But it is one that "could explain the very fast expansion of angiosperms around the globe," says Berendse.
They hope to test the idea further by examining the geological record for tell-tale signs that soil fertility did increase during the rise of the angiosperms, and that flowering plants initially came to dominate at lower latitudes, which should have had more nutrient-rich soils.