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THE only woody plant on Axel Heiberg Island is the dwarf arctic willow. Even
with its catkins flapping upwards in the chilly summer winds, the tiny tree
barely tops a hiking boot. But beneath the willow’s roots lies evidence that 45
million years ago the island’s vegetation was very different. Then, the hills
were covered in a lush forest of oak, sycamore and larch—home to flying
lemurs and the rhino-like Titanothere. The boggy lowlands were thick with swamp
cypresses and crawling with crocodiles and terrapins.

This isn’t just another example of plate tectonics changing the face of the
world. Axel Heiberg Island, in the Canadian Arctic, has moved no more than 2
degrees in tens of millions of years. But the transformation from temperate
woodland to arctic tundra holds the key to the disappearance of a primeval
forest that once extended throughout Asia, Europe and North America. It is also
the story of how the redwood family, which once dominated northern temperate
zones, was driven close to extinction, so that now all that remains is a handful
of giant sequoias and California redwoods in North America’s Pacific northwest
and a few isolated enclaves of dawn redwood and oriental swamp cypress in
China.

“It’s one of the most dramatic transitions in palaeobotany and I wanted to
know why it happened,” says Ben LePage, who has spent the last decade trying to
solve the mystery. In his cluttered office in the geology department at the
University of Pennsylvania, LePage holds up a sheet of rock containing the
fossilised remains of a tree. Fossils like this helped him discover that the
range of a whole group of trees, including redwoods, larches, ginkos and
sycamores began to shrink around the same time—between 40 and 35 million
years ago. He realised that the entire structure of the woodlands changed as
pines came to dominate the ecosystem. While species such as sycamores seem to
have survived the transition with most of their range intact, redwoods took a
body blow.

Exquisite clues

“Evidence from fossil wood, cones and pollen clearly shows that the pines and
redwoods coexisted for at least 100 million years,” says LePage. Throughout this
period pines were always a relatively minor component of the forest. Then 15 to
20 million years ago pine species suddenly took off. But this wasn’t a case of
an ancient group being ousted by a new competitively superior one. “The redwood
design worked well for over 60 million years,” he says. “What changed?”

LePage believes he now has an answer. And the first clue comes from Axel
Heiberg Island. At the base of the island’s Princess Margaret Mountain Range
lies Geodetic Hill, a hump shaped like a single teardrop. About two kilometres
long, it contains some of the most remarkable deposits of fossil plants in the
world. “The preservation is exquisite,” says LePage’s colleague, James Basinger
from the University of Saskatchewan. “It’s like looking at leaf litter on the
forest floor today.” They may be 40 million years old, but these remains are not
fossils. They have been effectively mummified. As a result of millions of years
of burial in an acidic, oxygen-free environment they are still organic, not
turned to stone but chemically and biologically intact.

Twelve seasons excavating these leaves, roots and tree stumps has let LePage
and his colleagues reconstruct the ancient landscape. “The plant communities
resembled those around a Louisiana bayou of today,” says Basinger. But there is
one crucial difference—the island’s trees would have endured complete
darkness for several months each Arctic winter. “It doesn’t seem to have harmed
them,” says Basinger. “Tree ring analysis shows their growth rates were as fast
as any temperate tree today.” Moreover, the abundance of swamp cypresses, which
won’t survive in freezing conditions, indicates that the climate was much warmer
then.

What once warmed this now frozen island? Throughout the late Cretaceous and
early Tertiary—between 70 and 45 million years ago—ocean circulation
patterns of the proto-Gulf Stream in the young northern Atlantic kept
temperatures high. Ocean currents brought warm water and moist warm air to
northern latitudes, much as the Gulf Stream does today. But because the land
masses had a different shape then, ocean circulation pushed tropical waters much
further north (see map).
The effects of this penetrating heat pump were
widespread. In Siberia, for example, much of what is now tundra was once a lush
forest, rich with redwoods. Then came some critical changes.

“Between 55 and 33 million years ago a seafloor rift was opening and
propagating northwards,” says Olav Eldholm from the University of Oslo. Until
about 38 million years ago the Arctic and Atlantic Oceans were separated by the
Greenland-Fennoscandian Ridge under the sea, and the Arctic’s isolated waters
were a thermal law unto themselves. Eldholm and Jorn Tielde from the Institute
for Marine Geoscience in Kiel have shown that the rifting created deep channels
on the seafloor, allowing cold, dense water from deep in the Arctic Ocean basin
to drain into the north Atlantic. The transition occurred over less than a
million years, according to evidence from the temperature-sensitive
ratio of the oxygen-16 and oxygen-18 isotopes in tiny fossil shells from the
seafloor. With this huge lens of dense cold water in place, patterns of ocean
circulation altered and the proto-Gulf Stream took on something approaching its
present circulation. The climate rapidly became cooler and drier. “For the
forests on Axel Heiberg the effects would have been catastrophic,” says LePage.
“The entire ecosystem probably collapsed in a short space of time.”

The cooling climate also affected the forests in the rest of North America
and Europe. Plants with a penchant for moist temperate climates that couldn’t
adapt to the changing environment had nowhere to go but extinct because the
rifting also sundered a series of land bridges joining North America and Europe.
So immigration could no longer supplement declining North American plant
populations, nor could they escape to the warmer climate of Europe from the
cooling regions in the north of the continent. The redwoods began a long slow
retreat.

Body blow

Trouble loves company, and the reeling redwood lineage was soon hit by
another body blow, the rise of the Rockies. “This had four major phases,” says
LePage’s departmental colleague Gomaa Omar. “The biggest occurred between 60 and
65 million years ago.” This would rapidly have added altitude to a predominantly
flat landscape, leaving large areas in the rain shadow of new mountains. LePage
believes these changes effectively trapped the American redwoods. “West of the
Rockies, their narrow environmental tolerance would have made the redwoods
unable to colonise or survive at the new mountains’ higher altitudes which were
colder and drier,” he says. “To the east, the new rain-shadow lands of the
Midwest would also have been unsuitable and tracts of redwood forest would
simply have shrivelled away.” In Asia, the final rise of the Himalayas, around
20 million years ago, likewise forced populations of dawn redwood and oriental
swamp cypress into ever smaller areas.

The rise of the Himalayas wrought immense changes which may have reshaped the
world climate—causing a cooling trend 55 million years long and initiating
the ice ages of the past 2 million years, according to MIT’s Maureen Raymo and
Bill Ruddiman of the University of Virginia. One important consequence was the
intensification of the monsoon weather system around 8 million years ago.
Gabriel Filippelli, a palaeoclimatologist at Indiana University, Pennsylvania,
has recently shown that an intensification of the Asian monsoon in the late
Miocene around 8 million years ago, triggered an upsurge in chemical weathering
on the Himalayan-Tibetan Plateau. This would have increased the drawdown of
atmospheric carbon dioxide which may well have caused the worldwide cooling from
the late Pliocene to the present and would, LePage believes, have hastened the
redwoods’ retreat.

Fatal flaw

But fate had not finished with the redwoods. The forest’s demise may have
triggered a feedback loop of increasing cooling and desiccation and further
forest loss. Computer modelling by Jan Dutton and Eric Barron of Pennsylvania
State University recently revealed that as trees were replaced by low-growing
grassland and tundra vegetation, more of the Sun’s energy would have been
reflected off the Earth’s surface. “In the summer the vegetation itself would
have had a higher reflectivity. In the winter it would have been the
snowfields,” says Barron. Snow would be slower to melt in spring and, with
moisture locked up in the snow and ice, drier conditions would prevail. Such
conditions would be a perfect breeding ground for grasses and hardy shrubs.

“All of which was obviously bad news for redwoods and their relatives,” says
LePage, “It partly explained the contraction of their range, but it didn’t
explain why pines replaced redwoods as the major northern temperate trees.”
Given the extent of the redwoods’ former range, LePage could not accept that
these mighty trees were incapable of genetic innovation. “You don’t last for
over 100 million years without some capacity to duck and dive. There had to be
some kind of Achilles heel that no one else had thought of.” He believes he has
now found the fatal flaw and, like many of the best discoveries, it involved
some serendipity.

In the early 1990s LePage’s first postdoctoral appointment was a study of
fossil fungi. “It certainly wasn’t my first love,” he says wryly. But the
experience proved fortuitous, giving him the background knowledge to explain why
redwoods have been overtaken so convincingly by pines. The answer, he believes,
lies in their roots. “Along with about 95 per cent of plants both pines and
redwoods are mycorrhizal, that is their roots possess a symbiotic fungal
association which is critical when getting nutrients out of the soil,” he says.
But LePage’s key realisation was that the two lineages have different types of
mycorrhizae. In redwoods the fungal strands have a deep and intimate association
with the tissues of the root—they are endomycorrhizal—whereas pines
are ectomycorrhizal, the fungal web sits near the root’s surface.

The next bit of the puzzle fell into place when LePage realised that these
two associations have different capacities for removing nutrients from the soil.
“In warm rainy environments phosphorus becomes very tightly bound to the
aluminium and iron hydroxides in the soil and is effectively unavailable to
plants. Then it is the limiting nutrient,” says LePage. “Up to 90 per
cent of a soil’s phosphorus can be locked up in this way.” The endomycorrhizal
fungi can ferret out this hidden bounty. Nitrogen becomes more difficult to
extract when the soil is acidic, or when the climate is very dry and or very
cold. This is when the pines come into their own because their ectomycorrhizae
excel at obtaining nitrogen.

“There is also a difference in the pH sensitivity,” explains LePage.
The fungi that form ectomycorrhizae perform best in acid soils where the
pH is 5.5 or lower. These conditions are common in cold areas where slow
decomposition rates result in the accumulation of humic acids which make the
soil more acidic. “In contrast, endomycorrhizal fungi commonly do best at
pHs of between 6 and 8,” says LePage. “Such alkaline soils are found in
places where decomposition is rapid, like redwood forests.” LePage concludes
that these mighty trees may have been brought low by their fungal associates.
“The two have probably been in an intimate physiological association for the
whole of their 100-million-year history. That’s a difficult bond to break.” The
more recently evolved pines, on the other hand, could benefit from
ectomycorrhizal associations which first appear on pine roots around 48 million
years ago. “At first it probably meant that they could inhabit the marginal
habitats unavailable to the more dominant redwoods. But, as the climate changed,
what was once marginal became mainstream, and the pine’s stock rose as a
result,” he says.

Limiting factor

It’s a very neat explanation. But there are some dissenting voices. David
Read, an expert on plant-fungal associations at the University of Sheffield,
agrees that ectomycorrhizae have been vital to the success of pines. “But I’m
not so sure about this idea with the redwoods,” he says. “I think the best you
can say is that it would be a contributing factor.” He points out that
endomycorrhizal associations don’t necessarily restrict a tree’s distribution.
The western red cedar, for example, extends right up into Alaska. “True, it
tends to occur on the better soils,” he admits, “but it does show that endos can
do it.” Read believes that the limiting factors for redwoods were mainly above
ground. As the climate became colder they would have found it increasingly
difficult to move water from the soil up into their high canopies, perhaps due
to a decreased rate of transpiration in the leaves.

“Of course, there will be exceptions,” responds LePage, “any flora comprises
a mosaic of plants with different nutrient acquisition strategies. Nothing in
biology is absolute. But cooler regions do tend to be dominated by
ectomycorrhizal species.” Neither does he accept that height was a critical
factor because on average, pines are taller than redwoods. “Sequoiadendron, the
giant redwood, and sequoia, the Californian redwood, are the only exceptions,”
he says. “If Read were right these once-widespread redwoods grew taller as their
ranges contracted.”

Despite such complications, LePage’s explanation for the fate of the redwoods
is generating excitement. “Its an elegant multi-disciplinary synthesis,” says
palaeobotanist Lisa Boucher, from the University of Nebraska. “This work has
revealed how key `choices’ in symbiotic relationships can strongly influence a
group’s evolutionary and ecological success.” It pays to choose your associates
wisely, it seems, because when the going gets tough they may let you down.