PERSPECTIVES
circulation models, and (ii) intermediate- with an increased AMO (16). This same
complexity models with zonally averaged
ocean components. Both suites of models
are known to be more sensitive to freshwa-
ter perturbations. In the first class of mod-
els, a small perturbation away from the
present climate leads to large systematic
errors in the salinity fields (as large flux
adjustments are applied) that then build up
to cause dramatic AMO transitions. In the
second class of models, the convection and
sinking of water masses are coupled (there
is no horizontal structure). In contrast,
newer nonflux-adjusted models find a
more stable AMO under future conditions
of climate change (11, 13, 14).
Even the recent observations of freshen-
ing in the North Atlantic (15) (a reduction
of salinity due to the addition of freshwater)
appear to be consistent with the projections
of perhaps the most sophisticated nonflux-
adjusted model (11). Ironically, this model
suggests that such freshening is associated
ECOLOGY
How Virgin
Is Virgin Rainforest?
K. J. Willis, L. Gillson, T. M. Brncic
onservation biologists increasingly
C use the term wild nature rather
than high biodiversity to identify
blocks of biodiverse habitats that have
been relatively undisturbed by human ac-
tivity (1). Their preference for this term is
driven by frustration that vast swathes of
biodiverse habitats continue to be lost at
unprecedented rates while biologists argue
about which currency is best for measur-
ing the value of biodiversitygenetics,
species, family, rarity, endemicityand
which regions should be selected for con-
servation efforts. This is especially true for
the tropical rainforests which, according to
current estimates, are disappearing at a rate
of ~6 million ha per year (2). Alongside
these depressing rates of destruction, evi-
dence has started to emerge from archaeo-
logical and paleoecological investigations
that many of these so-called virgin rain-
forest blocks might not be as pristine as
originally thought and have in fact under-
gone substantial prehistoric modification.
The implications of such studies for under-
The authors are in the Oxford Long-term Ecology
Laboratory, Biodiversity Research Group, School of
Geography and the Environment, University of
Oxford, Oxford OX1 3TB, UK. E-mail: kathy.willis@
geog.ox.ac.uk
402 16 APRIL 2004
3. B. Lemley, Discover 23, 35 (September 2002).
model proposes that it is only Labrador Sea
Water formation that is susceptible to col-
lapse in response to global warming.
In light of the paleoclimate record and
our understanding of the contemporary cli-
mate system, it is safe to say that global
warming will not lead to the onset of a new
ice age. These same records suggest that it
is highly unlikely that global warming will
lead to a widespread collapse of the
AMOdespite the appealing possibility
raised in two recent studies (18, 19)al-
though it is possible that deep convection
in the Labrador Sea will cease. Such an
event would have much more minor conse-
quences on the climate downstream over
Europe.
References
1. S. Rahmstorf, New Scientist 153, 26 (8 February
1997).
2. W. H. Calvin, Atlantic Monthly 281, 47 (January
1998).
standing the resilience and recovery of
tropical rainforests following human dis-
turbance are far-reaching and should not be
overlooked by conservation biologists.
The three largest undisturbed rainforest
blocks are in the Amazon basin, lowland
Congo basin, and the Indo-Malay region of
Southeast Asia (see the figure). Yet a num-
ber of case studies in each of these regions
now suggest that prehistoric human activi-
ties were far more extensive than originally
thought. In the Amazon basin, for example,
recent studies indicate that regions with the
most fertile soils in the lowland rainforest
are those with terra preta soils (3).
Formation of these soils is attributed to pre-
historic burning and agricultural activities
from around 2500 years ago, and in central
Amazonia, estimates suggest that terra pre-
ta soils cover up to 50,000 ha. In addition,
emerging archaeological evidence from the
Upper Xingu region of Brazil indicates ex-
tensive late prehistoric settlements dating
between ~1250 to ~1600 A.D., covering re-
gions up to 40 to 80 ha, and supporting
populations between 6 and 12.5 persons per
km2 (4). These were complex regional set-
tlements indicating intensive management
and development of the landscape and re-
sulting in large-scale transformation of the
forest to agricultural land and parkland.
VOL 304 SCIENCE www.sciencemag.org
4. IPCC, Climate Change 2001, The Scientific Basis.
Contribution of Working Group I to the Third Scientific
Assessment Report of the Intergovernmental Panel on
Climate Change, J. T. Houghton et al., Eds. (Cambridge
Univ. Press, Cambridge, 2001).
5. GRIP Project Members, Nature 364, 203 (1993).
6. A. J. Weaver, C. Hillaire-Marcel, Geosci. Can., in
press.
7. A. Berger, M. F. Loutre, Science 297, 1287 (2002).
8. D. C. Barber et al., Nature 400, 344 (1999).
9. A. Kuijpers et al., Mar. Geol. 195, 109 (2003).
10. C. Hillaire-Marcel, A. de Vernal, G. Bilodeau, A. J.
Weaver, Nature 410, 1073 (2001).
11. R. A. Wood, A. B. Keen, J. F. B. Mitchell, J. M. Gregory,
Nature 399, 572 (1999).
12. A. de Vernal et al ., Paleoceanography 17, 2:1
(2002).
13. P. R. Gent, Geophys. Res. Lett. 28, 1023 (2001).
14. M. Latif, E. Roeckner, U. Mikolajewicz, R. Voss, J. Clim.
13, 1809 (2000).
15. R. Curry, B. Dickson, I. Yashayaev, Nature 426, 826
(2003).
16. P. Wu, R. Wood, P. Stott, Geophys. Res. Lett. 31 (2),
10.129/2003GL018584 (2004).
Downloaded from www.sciencemag.org on March 31, 2015
17. E. P. Jones, Polar Res. 20, 139 (2001).
18. W. S. Broecker, Science 278, 1582 (1997).
19. R. B. Alley et al., Science 299, 2005 (2003).
Interestingly, abandonment of the land fol-
lowing catastrophic depopulation between
1600 and 1700 A.D. resulted in extensive
reforestation in many areas. The Upper
Xingu region of Brazil now comprises the
largest contiguous tract of tropical forest in
the southern peripheries of the Amazon.
A combination of archaeological and
paleoecological studies reveals a similar
story in the lowland Congo basin. Here,
there have been extensive finds of stone
tools, oil palm nuts, charcoal horizons
(subsoil layers of charcoal), banana phy-
toliths (silica bodies found in plants that
are preserved in sediments and permit
identification of the source plant), and pot-
tery fragments (5, 6). These discoveries
have led to the conclusion that much of this
region underwent extensive habitation,
clearance, and cultivation beginning ~3000
years ago and ending ~1600 years ago, fol-
lowing a population crash. In western cen-
tral Africa there is also archaeological evi-
dence for iron-working furnaces dating
from ~650 B.C.another activity that
would have had a serious impact on the
forest through the extraction of wood for
charcoal production and smelting. A popu-
lation crash in the fifth century A.D. re-
sulted in abandonment of the land and
widespread forest regeneration throughout
these regions (7). Many forest types result-
ing from this former human occupation are
still to be found in the lowland Congo
basin. In some areas, often considered vir-
gin, the forests may still be undergoing a
process of secondary succession (8).
There is even earlier evidence of prehis-
toric modification of the tropical rainforest
in the Indo-Malay rainforest block. This dis-
 PERSPECTIVES

Sou
Southern
outh Thailand d
Prehistoric
Preh
eh
h arboric
boriculture
ure
ree
and land
la m managem
anageme
nageme
ageme
gemen
emen
ment
ent
nt
from 800
000
00
0 yye
yea
years
ears
ars
rs
saag
ago
goo

Central Amazonia
maz
mazonia
zonia
Anthropogenic
Ant
Anthhropoge
oppogenic
terra preta soils
lss
from
m 355 years ago
500
Gabon
G
Iron-working furnaces
ace
e
from 961 B.C.

Papua
apua
ua New
N w Guinea
G
Agriculture
Agr culture from
fr
700
000 yye
years
ea ago
e

Upper Xingu River Region

Intensive management of
the landscape started
1250 to 1600 A.D.

Lowland Congo Bas sin

Stone tools, oil palm
mnnuts,
s,
banana phytoliths, and
nd
pottery fragments
from 3000 to 1600 years ago
New Georgia
Virgin rainforest
is 150 years old

Anthropogenic modification of virgin tropical rainforest. The map
indicates the three largest undisturbed rainforest blocks remaining world-
wide. These are located in the Amazon basin, the Congo basin, and
Southeast Asia (Indo-Malay region). Evidence is accumulating from ar-
chaeological and paleoecological studies that each of these regions had
been disturbed by prehistoric human settlements but had subsequently
regenerated once the populations moved on or died out. This suggests
that given sufficient time, tropical rainforests disturbed by modern human
activities may be able to regenerate.

turbance has affected the composition and
diversity of present-day species. Archae-
ological and archaeobotanical evidence sug-
gest that agriculture (including the cultiva-
tion of bananas) was established ~7000
years ago in Papua New Guinea (9) and that
the lowland rainforests of Thailand have
been managed from as early as 8000 years
ago. In the rainforests of Thailand, human
occupation and management of the land
may have increased tree diversity (10).
Finally, in the Solomon Islands, evidence
from archaeology, ecology, and oral history
suggests that the population of New Georgia
in 1800 may have been twice that of today,
with settlements of up to 7000 people. Thus,
this apparently pristine island rainforest may
be a consequence of regeneration over the
past 150 years, following population decline
and migration to coastal regions (11). The
enrichment of these present-day island rain-
CREDIT: PRESTON HUEY/SCIENCE
acceptable to suggest that land loss caused
by previous human activities was too small
to have had a major impact and therefore
cannot be compared to present-day losses.
This point is reinforced by current esti-
mates suggesting that the main agent of de-
forestation in the tropical forests, account-
ing for up to two-thirds of the annual loss,
is slash-and-burn farming (12). Thus, al-
though the rate and extent of forest clear-
ance might be much greater today, in many
cases, the process is comparable to prehis-
toric losses. Second, in most examples of
prehistoric disturbance there was subse-
quent forest regeneration. These tropical
ecosystems are not as fragile as often por-
trayed and in fact are quite resilient. Left for
long enough, forests will almost certainly
regenerate. Third, a long-term paleoecolog-
ical record enables realistic estimates to be
made about the time it takes for a forest to
vation of newly cleared regions and should
be routinely incorporated into restoration
planning. These approaches have been suc-
cessfully applied to conservation of mid-
latitude forests (13) but have yet to be ap-
plied systematically to some of the most di-
verse but threatened forests on Earth.
References and Notes
1. A. Balmford et al, Science 297, 950 (2002).
2. F. Achard et al, Science 297, 999 (2002).
3. B. Glaser, L. Haumaier, G. Guggenberger, W. Zech,
Naturwissenschaften 88, 37 (2001).
4. M. J. Heckenberger et al., Science 301, 1710 (2003).
5. L. J. T. White, African Rain Forest Ecology and
Conservation, B. Weber, L. J. T. White, A. Vedder, L.
Naughton-Treves, Eds. (Yale Univ. Press, New Haven,
CT, 2001), p. 3.
6. C. M. Mbida et al., J. Arch. Science 27, 151 (2000).
7. R. Oslisly, African Rain Forest Ecology and Con-
servation, B. Weber, L. J. T. White, A. Vedder, L.
Naughton-Treves, Eds. (Yale Univ. Press, New Haven,
CT, 2001), p. 101.
8. T. van Gemerden et al., J. Biogeogr. 30, 1381 (2003).
9. T. P. Denham et al., Science 301, 189 (2003).

forests in secondary tree species adds fur-
ther support to this possibility.
Beyond pure interest in the antiquity of
tropical rainforests and how humans may
have shaped them, these studies have im-
portant implications for conservation biolo-
gy. First, they indicate that it is no longer
regenerate after abandonment. It also pro-
vides a quantitative assessment of forest
composition before and after disturbance,
providing detailed information on what is
missing from, or added to, the forest when
it regenerates. Such information is critical
to the management and long-term conser-
10. L. Kealhofer, Asian Perspect. 42, 72 (2003).
11. T. Bayliss-Smith et al., Ambio 32, 346 (2003).
12. N. Myers, Protecting the Protected: Managing
Biodiversity for Sustainability, T. ORiordan, S. Stoll,
Eds. (Cambridge Univ. Press, Cambridge, UK, 2002), p.
46.
13. D. R. Foster, J. Biogeogr. 29, 1269 (2002).
14. We thank K. D. Bennett for helpful comments.

www.sciencemag.org SCIENCE VOL 304 16 APRIL 2004 403

 How "Virgin" Is Virgin Rainforest?
K. J. Willis et al.
Science 304, 402 (2004);
DOI: 10.1126/science.1093991

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