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This year some 100 000 square kilometres of pristine rainforest – an
area roughly the size of Iceland – will be burnt to the ground to produce
farmland. A further 50 000 square kilometres will be invaded by logging
companies intent on extracting timber of high commercial value. Nobody doubts
that the burning will cause irreversible destruction, of both trees and
wildlife. But what of the logging?

The conventional view of timber extraction is that it is the kiss of
death for a rainforest. Loggers move in with their roads and heavy tractors,
remove the most valuable timber and then abandon the forest, depleted, to
slash-and-burn farmers. But does it have to be like this? The International
Tropical Timber Organisation, a trade association set up by the 47 nations
of the world that either produce or import tropical timber, thinks not.
Driven by public concern and necessity – many of the world’s rainforests
will be exhausted within two decades if things do not change – ITTO has
become an evangelist for sustainable logging. It has set itself the target
of making responsible, ‘scientific’ logging the norm throughout the tropical
world by the year 2000.

Many environmentalists remain profoundly sceptical. They point to the
ITTO’s abysmal track record on policing the timber industry and the fact
that less than 0.1 per cent of the world’s rainforest is at present under
any form of sustainable management. Everyone agrees that without enormous
political will this situation is unlikely to change. But even if the will
is there, how can we be sure that any future logging practices dubbed ‘sustainable’
by the timber industry really do allow rainforest the chance to regenerate?

Underlying this question are some thorny scientific problems. Just how
resilient are rainforests to small-scale disturbances? How fast can they
repair gaps in their canopies? And what, if any, is the ecological value
of the ‘secondary’ vegetation which often emerges after a rainforest has
been logged?

Five years ago we set about finding some answers in Borneo, home to
one of the world’s richest rainforests. We joined a team of scientists from
Britain and Southeast Asia at the Royal Society’s field station in Danum
Valley, Sabah, one of the most heavily logged regions of Malaysia. Our mission
was to study the impact on a small area of rainforest – its vegetation,
microclimate, wildlife, insects and so on – of creating holes in its canopy.
Recently we met other botanists and ecologists at the Royal Society in London
to discuss in detail what we have found so far.

Tropical rainforest is commonly perceived as one of the most ancient
and stable ecosystems on Earth. Yet even virgin, or primary, rainforest
suffers much natural disturbance by, for example, hurricanes, landslides
and even droughts. During the past decade, for example, tracts of primary
rainforest in Borneo and Brazil were destroyed by fires brought on by drought.
The great fire of Borneo in 1983 destroyed some 40 000 square kilometres
of forest, a vast area given that the present rate of logging there is about
7000 square kilometres per year. Much more common, though, is disturbance
of a less drastic kind – the tiny gaps that appear in a forest canopy whenever
a tree dies and falls over. Anyone who has camped overnight in a rainforest
will have been startled from time to time by a nearby tree crashing to the
ground. Far from destroying the forest, such natural disturbances provide
opportunities for regeneration. An entire rainforest can turn over in not
much more than 120 years.

If rainforests can recover from natural disturbances, why not from logging?
Presumably the odds on recovery will be shortest when the gaps are small.
But exactly how small is small, and to what extent does the size of a gap
influence the speed and quality of forest regeneration? These questions
lie at the core of a branch of biology known as forest dynamics, and they
underlie much of our work in Sabah.

Forest dynamics is by no means a new subject. For several decades, biologists
have studied forest regeneration in the natural gaps formed by the everyday
collapse of ageing trees. One factor more than any other seems to determine
the pattern of regrowth: the amount of sunlight the gap allows in through
the forest’s evergreen canopy. When it is completely intact, the canopy
– which can be up to 30 metres deep – absorbs most of the sunlight, leaving
the forest floor cool, moist and dark. So intense is the shade, in fact,
that the banks of seedlings which cover the rainforest’s floor find it hard
to grow.

Most of these seedlings are of so-called climax species, trees such
as the dipterocarps which predominate in primary rainforest in Southeast
Asia and provide valuable hardwood timber. Their seeds are produced almost
continuously and germinate immediately. But in the deep shade of the forest
floor, most of the resulting seedlings remain suppressed for years, scarcely
growing at all. The tiniest hole caused by a branch falling may be enough
to trigger the growth of a climax seedling from the forest floor. Yet give
such a seedling too much sunlight and it will soon wither.

The risk of overdosing on light is not the only problem climax seedlings
face in their struggle to reach maturity. They must also contend with stiff
competition from another class of tropical plant: fast-growing trees with
soft, low-density wood, known as pioneers. One such adversary is balsa,
a pioneer species from Central America which can grow at up to seven metres
a year. Unlike their climax counterparts, the seeds of pioneers can remain
dormant in soil for years and usually germinate only after being activated
by sunlight or heat. Also in contrast to climax seedlings, pioneers thrive
in bright light. So in open sunny gaps, or following slash-and-burn clearance
of a forest, pioneer vegetation soon emerges and dominates. A gap produced
by the deaths of four or five adult trees allows at least 20 times as much
sunlight to reach the forest floor – more than enough to stimulate the germination
of pioneers.

Grouping tropical trees into light-loving pioneers and shade-adapted
climax species is the starting point for understanding forest dynamics.
But this simple division conceals many complexities, not least the question
of how rainforests evolved, and continue to sustain, such an exuberance
of plant life. A single hectare of Peruvian rainforest contains on average
eight times as many species of tree as the whole of Britain. How can so
many species coexist without a large proportion being driven to extinction?
Why are there so many apparent winners in the competition for light, water
and mineral nutrients? Answering this puzzle holds the key to developing
strategies for exploiting rainforests sustainably.

Competing theories abound. One hypothesis, championed by the Costa Rican
ecologist Dan Janzen in the mid-1980s, points to pressure from predators
as the driving force behind rainforest diversity. Each time a herbivore
species evolves protection against the chemical or mechanical defences of
a plant, there will be evolutionary pressure on plants to evolve further
defences. It is this biological arms race which, supposedly, ensures a constant
turnover of new and more varied species of both plant and predator. The
idea is sometimes called the Red Queen hypothesis in honour of the passage
in Alice Through the Looking Glass where the queen tells Alice: ‘It takes
all the running you can do to stay in the same place.’

A second school of thought ascribes the diversity of tropical ecosystems
to the effects of natural disturbances. The most extreme theory of this
kind is the so-called refugia hypothesis, which points to the climatic turmoil
of the Pleistocene (between 1 and 2 million years ago) as the dominant source
of disturbance. As glaciation advanced over the northern continents during
that period, it argues, rainfall in the tropics diminished, with the result
that what were previously whole forests temporarily fractured into islands
– or refuges – of forest separated by arid areas. Life within these refuges
then rapidly diversified; when they later merged the resulting habitats
were rich in species and have remained so ever since. That, at least, is
the speculation.

In principle diversity may also be the product of less drastic disturbances
to rainforest habitat, such as damage caused by landslides, earthquakes,
rivers switching course, or even the collapse of aged or diseased trees.
This is the basis of the so-called gap dynamics theory. The idea here is
that the conditions prevailing in gaps of different sizes favour different
species of tree. Hence each climax species is uniquely adapted to grow in
a gap of one particular size. Moreover, because gaps caused by natural disturbances
must vary in size, many different species of tree are encouraged to regenerate.
Variety in gap size is the driving force behind biological diversity in
the rainforest – or so the hypothesis holds.

Testing these theories has proved quite a challenge for tropical ecologists.
What limited data there are seem to cast doubt on the importance of predator
pressure, but the theory still has its committed disciples. Similarly, the
evidence for the refugia hypothesis remains far from conclusive. Its critics
point to the fact that many, if not most, rainforest species are distributed
uniformly, rather than in clumps. Meanwhile, in the absence of any evidence
at all, it has been the gap dynamics theory that has appealed most to ecologists.
Only with our work in Sabah has that theory finally been put to the test.

What we did in Sabah was to cut a series of precise holes in the canopy
of the Danum Valley rainforest. These varied in size from 10 to 1500 metres
square, and during the following four years we carefully recorded the fate
of each climax seedling growing on the exposed forest floor beneath the
holes. Most of the work was done with Tim Whitmore, a rainforest ecologist
from the University of Oxford.

As expected, many of the climax seedlings in the largest gaps were scorched
by strong sunlight and died within a few weeks. Others struggled on only
to be massacred by shoot borers and other insects at a later stage. The
survivors of this onslaught appeared unable to continue growing upwards,
so the gaps soon filled with sprawling bushes. As we monitored the fates
of climax seedlings, Don Kennedy and Mike Swaine of the University of Aberdeen
kept tabs on the pioneers. Although these germinated in gaps of many different
sizes, only in the larger gaps – formed by the removal of two or more canopy
trees – was there enough sunlight for pioneer seedlings to survive more
than a couple of years.

The most surprising finding came from the smaller gaps. At the outset
we had expected gaps of different sizes to favour different climax species,
in line with the gap dynamics theory. Yet our results provided scant evidence
of this. What seemed to matter most was simply seedling height. Initially,
each gap was populated by a variety of seedling species, all of very different
ages and sizes – the survivors of many years of suppression by forest shade.
But in due course it was the seedlings that were tallest to start with –
regardless of species – which went on to dominate the gap. The smaller seedlings,
even if they were able to grow faster than their taller colleagues in bright
light, were unable to catch up before the ground became shaded by the expanding
canopy of the tall seedlings.

The tallest seedlings were usually of species such as Hopea nervosa,
which can grow slowly in deep shade for many years. The seedlings of species
less well adapted to shade, such as Parashorea malaanonan, were younger
and shorter. The gap dynamics theory overlooks this type of variation in
the seedling bank, which may explain why our results appear at odds with
its predictions. At the same time, our findings raised a new puzzle: why
do climax species which can survive deep shade not drive to extinction those
that need light to grow?

We think the reason lies not in the different sizes of natural gaps
but in a completely different variable: how frequently a rainforest canopy
is opened up. Even the tiniest gap in the canopy substantially improves
the survival prospects of seedlings that cannot grow in deep shade. So in
areas of forest which are especially prone to disturbance, shade-adapted
seedlings will lose their competitive advantage over seedlings that cannot
grow in shade. The spells between disturbances are simply not long enough
for them to gain a head start. The more frequently the canopy is opened
up, the more the two kinds of seedlings would approach competitive equality.

In some circumstances, the initial inequality may even reverse itself,
because extreme tolerance to shade must involve at least some physiological
compromises. Greenhouse studies in Costa Rica and Sabah show that in sunny
conditions shade-adapted climax seedlings are generally outpaced by seedlings
that struggle to survive in deep shade.

Taken together, our results sound a cautionary note for rainforest management.
At present the vast majority of logging operations around the world create
large gaps in canopies. Figures from the Amazon and Southeast Asia indicate
that as many as 70 per cent of trees in a forest may be damaged or destroyed
to extract only 10 per cent of them. To make matters worse, bulldozers and
caterpillar tractors often crush the forest’s banks of climax seedlings.
Even when logging is done selectively, careless forestry practice generally
destroys at least half the canopy. Only pioneer species are able to cope
with the resulting brightness, heat and low humidity.

There are no easy solutions. Unless logging companies eliminate all
unnecessary damage, they will have to reduce drastically the amount of timber
they extract. If climax species are to be given any chance of regenerating,
loggers must open up no more than 25 per cent of the canopy during each
cut. Even then, the biological diversity of the forest will be at risk.
To extract timber in a way that is both commercially and ecologically sustainable,
logging companies must go a step further. They must try and mimic the natural
disturbances that help to sustain biological diversity, and avoid patterns
of activity that erode it. This means varying not only the sizes of the
gaps they make but also how often they disturb different parts of the forest.

But the news is not all bad. Pioneer vegetation may be of lower biological
diversity than primary rainforest, and its soft timber may be of low commercial
value, but its speedy growth in a logged rainforest can play a vital part
in restoring the damp, cool conditions necessary for climax trees to re-establish
themselves. What is more, according to research by Ian Douglas and his colleagues
from the University of Manchester, pioneer trees can also help to check
the soil erosion that occurs when logging exposes forest land. Following
a commercial cut in Sabah, the researchers found that the sediments in a
stream draining the logged forest had increased 18-fold; but a year later,
after pioneers had colonised the area, the sediments had fallen to less
than four times the normal level.

Research on the impact of logging on wildlife gives room for optimism,
too. Contrary to expectations, Andy Johns and Frank Lambert, of the University
of Aberdeen, have found that few species of vertebrate are lost entirely
when a rainforest is logged, though the local populations of some vertebrates
plummet. In their study, large herbivores such as elephants and deer positively
thrived on pioneer vegetation. The creatures that fared least well were
those with highly specific food needs. Woodpeckers and flycatchers, for
example, became confined to whatever small pockets of untouched forest remained
after logging. Primates were also hard hit. The local orang-utans had few
young for several years after the forest had been logged.

A similar story is emerging from the work of entomologists Jeremy Holloway
of the Natural History Museum and Ashley Kirk-Spriggs of the National Museum
of Wales. On the positive side, logging appears to leave relatively unscathed
those insects such as dung and carrion beetles that can exploit a wide range
of food resources. But the local populations of insects such as moths, which
feed on highly specific rainforest plants, tend to crash.

All these results, however, paint what is probably an idealised picture.
Logging invariably provides road access for hunters and migrant farmers
who often devastate the local wildlife. Moreover, our knowledge of the intricate
web of biological interactions that sustains a rainforest is still far from
complete. A key unanswered question is the extent to which long-term fluctuations
in the populations of pollinators, seed dispersers and herbivores affect
the composition of a logged rainforest. What good does it do to preserve
a forest’s capacity to regenerate its trees if logging has driven away the
animals that disperse their seed?

What we do know is that natural disturbance is central to the life cycles
of all rainforests, and that to get close to mimicking it, logging companies
will have to reduce the size of the gaps they make in canopies. Yet, as
our project also reveals, size isn’t everything: the success of the healing
may also depend on the frequency with which the woundsare inflicted.

Nick Brown is a rainforest ecologist who lectures in the Department
of Geography at the University of Manchester.

Malcolm Press is a plant physiologist who lectures in the Department
of Environmental Biology at the University of Manchester.

* * *

Rainforest plants that grow in the dark

How do tree seedlings survive the dense shade of a tropical rainforest?
For years botanists struggled with this question helped only by clues from
laboratory experiments on plant species that are often ill-equipped to withstand
shade. These days botanists go to the forest floor to do their experiments;
only there can they investigate the crucial role of sunflecks.

Only about 2 per cent of the light falling on a rainforest canopy reaches
the forest floor. Of this, about three-quarters is in the form of sunflecks
– unfiltered sunlight that has not passed through leaves higher up in the
canopy. When these flecks hit the forest floor, leaves may be brightly lit
for anything from a few seconds to more than half an hour.

Botanists are studying how rainforest leaves respond to sunflecks by
measuring the rates at which they fix carbon dioxide. How much carbon dioxide
a plant consumes is governed by the intensity of the light falling on its
leaves. In darkness, there is no carbon fixation, only respiration, and
in this state plants are net producers, rather than absorbers, of carbon
dioxide. As the intensity of light increases there comes a point – the ‘compensation’
point – when the amount of carbon dioxide released by respiration equals
that fixed by photosynthesis. In the ‘understorey’ of the rainforest, plants
have low compensation points: they minimise the amount of carbon dioxide
lost through respiration and maximise the amount of carbon dioxide they
can absorb in shady conditions.

Botanists have long known that the dark green leaves of rainforest plants
are unusually efficient at capturing sunlight. Not only have the leaves
adapted their shapes to optimise light capture, but the molecular machinery
with which they carry out photosynthesis is also highly responsive.

More recently, researchers have been trying to answer another question:
have rainforest plants evolved to be more responsive to sunflecks than to
continuous radiation? Robin Chazdon and Robert Pearcy of the University
of California at Davis think the answer is yes. Their research shows that
plants from shady habitats capture sunflecks more efficiently than plants
from sunny habitats.

When light hits darkened leaves there is a time lag, or induction phase,
before it boosts the rate of photosynthesis in the leaves. It seems that
in rainforest plants, pulses of light – simulated sunflecks – are just as
good at getting photosythesis going as continuous light. When photosynthesis
is in full swing in a plant’s leaves and the intensity of light suddenly
falls, the rate of photosynthesis will begin to decline exponentially. Chazdon
and Pearcy found that this decline occurs much more slowly in the leaves
of rainforest understorey species than in light-demanding plants. Thus,
the effects of sunflecks outlast their duration, allowing carbon dioxide
to be fixed in the darkness that follows a sunfleck.

Botanists are now investigating whether these results apply to a range
of other understorey plants, while biochemists try to uncover the molecular
processes that allow rainforest plants to continue to fix carbon dioxide
long after the sunfleck has passed.

Sunflecks, and the varying abilities of different species of plants
to capture them, may also explain why some climax seedlings survive longer
than others under the canopy, and so get a head start on competitors when
a gap forms.

In large gaps the very strategies that enable climax seedlings to survive
in deep shade turn out to be their downfall. Their shade-adapted leaves
do not have the biochemical machinery needed to harness what can be as much
as a hundred-fold increase in light energy. As a result they soon become
overloaded or ‘photodamaged’, a condition which usually leads to leaf bleaching
and, eventually, death.

Plants which live on the forest floor are not only shaded from light,
but also from extremes of desiccation, temperature and wind. Our remaining
problem is to work out exactly what such changes mean for the seedlings
of climax species such as the dipterocarps. Only with such information in
hand will we be able to understand properly the role of gaps in seedling
regeneration, and design logging regimes compatible with the sustainable
use of tropical forests.