ELS EVI ER 0 0 0 6 - 3 2 0 7 ( 9 5 ) 0 0 1 2 2 - 0

Biological Conservation 76 (1996) 219228

Copyri ght (C 1996 Elsevier Science Limited
Printed in Great Britain. All rights reserved
0006-3207/96/$15,00+0.00
AMAZONI AN CONSERVATI ON IN A CHANGI NG WORLD
Mark B. Bush
Department of Botany, Duke University, Durham. NC 27708, USA
(Received 1 March 1994; accepted 3 September 1995)
Abs t ract
Prioritization of areas f or conservation in Amazonia is
based on estimates of modern biodiversity and the distri-
bution of endemic species. The refugial hypothesis pro-
vided an important conceptual basis f or understanding
the effects of climatic" change on these reserve areas. The
hypothesis predicted that ice-age aridity in Amazonia
would have been the dominant f orce that resulted in mod-
ern patterns of endemism. However, recent paleoecologi-
cal data indicate that cooling, rather than drying, was the
predominant climatic influence on the ice-age Amazon
,forests, and this leads' to a re-evaluation of forces structur-
ing Amazonian diversity patterns. Modern Jorest clearance
may result in a warmer and drier Amazon basin," conditions
non, seen to be without past analog. In the light of these
data, assumptions regarding the survival o f f orest isolates
in a drying landscape must be revised. Habitat functions
in the sense of hydrogeomorphic processes and climate are
recommended as conservation goals rather than explicitly
attempting to save biodiversity. Reserve areas should be
established in the expectation of f ut ure climatic change
and be large enough to allow the ensuing migration of
species. Copyright 1996 Elsevier Science Limited.
Keywords: Amazoni a, biodiversity, climatic change,
conservation, Holocene, hydrol ogy, Pleistocene, paleo-
ecology, refugia.
I NTRODUCTI ON
The goal of most conservationists is to mai nt ai n as
much biodiversity as possible, even when substantial
areas of forest are convert ed for economi c use (Gins-
burg, 1987; McNeel y, 1992; Western, 1992). Unlike the
more developed nat i ons who have al most not hi ng left
to protect, nat i ons with Amazoni an territories still have
the choice of where to locate nat ur e reserves, how
extensive t hey shoul d be and how many should be
established. In Amazoni a, the oppor t uni t y to establish
wildlife reserves may not arise again, for once develop-
ment has started in an area, wresting l and from com-
peting uses is virtually impossible. Recognizing the
i mport ance of pl anni ng reserves before the area is
Correspondence to: Mark B. Bush. Tel.: (919) 684 4003; Fax:
(919) 684 5412; e-Mail: mbush@acpub.duke.edu
developed, the countries sharing Amazoni a have each
established conservat i on areas. This pl anni ng has t aken
account of phyt ogeographi c variability, and biodiver-
sity. However, for these plans to be successful in the
long term, hydrol ogi cal and climatic regimes must be
mai nt ai ned at bot h a local and regional scale. The true
value of the reserves lies in their existence for perpetuity,
and therefore, they should be planned to accommodat e
as much climatic and environmental change as possible.
Present estimates of Amazoni an deforest at i on sug-
gest t hat about 6% of the nat ural forest cover has been
replaced with degraded forest or grassland (Skole &
Tucker, 1993). However, fragment at i on of once
forested areas and the area indirectly affected by defor-
estation t hrough ' edge effects' (Lovejoy et al., 1986),
doubles the area of Brazilian Amazoni a di st urbed by
devel opment to about 12% (Skole & Tucker~ 1993).
Conservat i on pl anni ng must encompass the likely
short -t erm prot ect i on of sites from fragment at i on, and
the edaphic and erosional consequences of deforesta-
tion (Fearnside & Ferreira, 1984~ Myers, 1988). Plan-
ners must also look to longer time-scales to estimate
the robustness of proposed reserve structures given
global climate change on a millennial scale. If we do
not intend to save reserves in perpetuity there seems lit-
tle point in starting to set aside any l and for nat i onal
parks. Therefore, the reserves must be designed to
wi t hst and the scale of climatic change, ant hropogeni c
and nat ural , t hat can be predicted.
PREDI CTI ONS OF CLI MATI C CHANGE IF
AMAZ ONI A IS DEFORESTED
The local effect of deforest at i on is to increase greatly
surface soil temperatures, reduce moi st ure availability
in the upper horizons, extend the length of dry seasons,
and hence increase soil water deficits (Dickinson, 1991:
Salati & Nobre, 1991; Saunders et al., 1991). An
increasingly xeric upper soil envi ronment may lead to a
general decrease in evapot ranspi rat i on, with a conse-
quent loss of local humi di t y, and reduced precipitation
(Salati et al., 1979). Reduced humi di t y may also
decrease cloud cover, which could lessen albedo and
lead to heating, or decrease the insulation and lead to
cooling (Lean & Warrilow, 1989; Salati & Nobre,
1991). Furt hermore. changes to surface texture, a
219
220 M . B . B u s h
feature with strong correlation with predicted climatic
change in General Circulation Models (Pitman e t a l . ,
1993), are also likely if humid forests are replaced by
more xeric forest or savanna.
If these patterns of local climate and vegetation
change are repeated over a wide enough area, the cli-
mate and hydrology of the whole Amazon basin may
be altered. Salati e t a l . (1979) estimate that as much as
50% of regional rainfall in Amazonia is due to local
evapotranspiration and re-precipitation. Comput er sim-
ulations for an Amazonia reduced to pasture suggest a
1-3C warming, a 26% reduction in precipitation, and
evapotranspiration reduced by 38% (Shukla e t a l . ,
1990). A GCM simulation of a 6-year period under
conditions in which Amazonia is deforested suggests a
more modest warming, about 0.69C (Pitman e t a l . ,
1993), but similar reductions in precipitation and evapo-
transpiration to the estimates of Shukla e t a l . (1990).
The effect of global warming, as a result of atmo-
spheric enrichment by greenhouse gases, is likely to be
accelerated by widespread Amazonian deforestation
(Eden, 1990) and may increase Amazonian tempera-
tures by I ~ C within the next century (Goddard Insti-
tute for Space Studies, pers. comm.). Such a change
would exacerbate existing drought stress and lead to
the expansion of xeric habitats at the expense of moist
forests. The forests most likely to be affected are those
that are ecotonal, forming the boundary between moist
rainforest and cerrado; a boundary that is most often
water- or fire-dependent (Eden, 1990).
HOW MUCH LAND MUST BE SAVED, AND IN
WHAT CONFI GURATI ON?
Nat ure reserves and national parks often function as
islands within a sea of development, and hence island
biogeography plays a considerable role in determining
optimum size and arrangement of reserves (Diamond,
1976; Sharer, 1990). Based on MacArt hur and Wilson' s
(1967) theory of Island Biogeography, it has been sug-
gested that if 50% of an area is maintained as natural
vegetation, most species can persist (Odum & Odum,
1972). However, the area required to save different
groups of organisms is likely to vary considerably. In
Norwegian forests, maintaining avian biodiversity
required about one-quarter of the land area needed to
safeguard all plant species (S~etersdal e t a l . , 1993).
Insects are such an important component of tropical
forest biodiversity (Wilson, 1992) that they should
figure centrally in conservation planning. As insects are
often chemotaxonomically restricted to a particular
host foodplant, maintaining insect diversity may
require areas similar to those needed to protect plant,
rather than bird, diversity. Furthermore, the study of
Norwegian forests, like many biogeographic studies,
was based on species presence, not on sustainable pop-
ulations, nor on the likelihood of survival given contin-
ued global climate change (S~etersdal e t a L , 1993). The
massive diversity and individual rarity of species within
neotropical forests (Richards, 1952) would tend to
increase the percentage of the total area that must be
protected in order to include all species, and to protect
them through time.
Forest fragmentation by development requires plan-
ners to consider the arrangement of reserve lands, a
dilemma summarized as SLOSS (Single Large Or Sev-
eral Small; e.g. Diamond, 1976; Simberloff & Abele,
1976; Terborgh, 1976). The fear exists that if t oo few
reserves are established, the spatial arrangement may
preclude the inclusion of all habitat types, phytogeo-
graphic units, or endemic populations. If small reserves
are chosen they may include the full diversity of the
biota but they may not be large enough to maintain
minimum viable populations of all species (Diamond,
1976; Terborgh, 1976). Examples of the loss of species
following the isolation of an area, termed ' relaxation'
are many, e.g. the loss of j aguar and tapir and c.
25-30% of bird species from Barro Col orado Island,
Panama, since 1913 (Willis, 1974). The sheer species
diversity of Amazonian forests dictates that individual
reserves must be large. Estimates of minimum areas to
support populations have been as low as 100,000 ha
needed to maintain avifaunal biodiversity (Willis,
1979), to more than 250,000 ha required to maintain
full faunal and floral diversity (Terborgh, 1974; Myers,
1979; Higgs & Usher, 1980; Terborgh & Winter, 1980).
Most recently, it has been suggested that a minimum
size for individual reserves should be 1 - 2 million ha if
full biodiversity and heterozygosity of large predators
is to be maintained (J. Terborgh, pers. comm.). These
estimates assume a constant environment; none includes
a parameter for future climatic change.
It is politically unlikely that Amazonian forests can
be saved in their entirety, so it falls upon the planners
to identify areas for varying degrees of development.
International pressure, and a growing domestic aware-
ness of the resource that they hold, has spurred the
Brazilian government into a series of initiatives
designed to prioritize areas for conservation. In 1"965,
legislation was established in Brazil to ensure that 50%
of Amazonia was maintained with some kind of forest
cover (Pandolfo, 1974; Goodl and & Irwin, 1975).
Since then land quotas have been suggested for zoning
Brazilian Amazonia that provide c. 150 million ha (40%
of Amazonia) as wildlife areas, 110 million ha (29%)
for forestry and agro-forestry, 70 million ha (18%) for
Indian lands, and 50 million ha (13%) for agricultural
colonization (Dub& 1980). Just as 50% of Amazonian
land is unlikely to be protected, so t oo is the 40% sug-
gested by Dub6 (1980); a more conservative estimate is
that 15-20% may eventually be designated as National
Parks (Pandolfo, 1974: Myers, 1979, 1984). At present
just 4% of Amazonia lies within National Parks
(Eden, 1990).
Since the mid-1970s the Brazilian government has
requested the aid of ecologists and biogeographers in
A m a z o n i a n c o n s e r v a t i o n 221
helping to identify and prioritize further conservation
areas. This action should be lauded as it signifies a
commitment to a thoughtful and planned development
of Amazonia.
CONSERVATION AND THE REFUGIAL
HYPOTHESIS
The proposed conservation areas in Brazilian Amazo-
nia have been raised on the perceived distribution of
endemic species. A lesser, but still central, construct for
defining these areas has been the concept of the exis-
tence of Pleistocene refugia. The refugial hypothesis
(Hailer, 1969) proposed a speciation model for Amazo-
nia that sought to explain pockets of high species
endemism among birds. The hypothesis suggested that
during the Pleistocene ice-ages Amazonia became dry
- - t oo dry to support tropical rainforest - - and that in
its stead great grasslands developed. Only a few refugia
of tropical rain forest remained as islands in a sea of
savanna. These isolates were in the wettest locations,
either along the western flank of the Amazon basin, or
on elevated ground. Hilltops tend to be wetter than the
adjacent lowlands because of precipitation due to oro-
graphic rainfall, and thus the refugia frequently coin-
cided with high ground. Implicit assumptions of the
' Refugial Hypothesis' were ( 1) t ha t modern endemic
patterns result from Quaternary speciation events; (2)
that refugia contained unchanging forests of lowland
taxa t hroughout the Quaternary; (3) that Amazonian
temperatures at the last-glacial maximum were within
2C of present; (4) that precipitation was reduced suffi-
ciently to fragment the forests; and (5) that reduced
gene flow resulted in allopatric speciation.
Refugialists argue that the isolated forests were arks
for the plants and animals of the rainforest, were genet-
ically disjunct from other forest areas, and were sites of
allopatric speciation. With the return of moist inter-
glacial conditions, the forests spread across Amazonia
and ousted the grasslands, but the signature of the
refuge was still evident in the high proportions of
endemic species on the hilltops relative to the interven-
ing areas. This hypothesis was so attractive that numer-
ous biogeographers have analyzed their data sets in a
similar manner and produced patterns of refugia. Dat a
for nymphalid butterflies (Brown, 1982, 1987a), A n o l i s
lizards (Vanzolini, 1970; Vanzolini & Williams, 1981),
amphibians (Duellman, 1972, 1982), stingless bees
(Camargo, 1978), scorpions (Lourenco & Florez, 1991),
and some plant families (Prance, 1982, 1987) have been
presented as refugial maps for the last ice-age. By
amalgamating these data it was assumed that the
greater the concordance of the patterns, the stronger
the definition of the refugial boundary. Geomorphol og-
ical evidence was also raised to support the refugial
hypothesis. Buried stone-lines beneath the terra firme
forests of Amazonia were suggested to have been
formed during times of reduced vegetation and aridity
(Tricart, 1974; Journaux, 1975). Ab' Sfiber (1982) sug-
gested that the stone-lines were formed during a single
widespread period of aridity during the terminal Pleis-
tocene, and that the presence of white sand soils and
sand dunes within the Amazon basin has also been tied
to dry events in the Quaternary. As these deposits were
undated, their relationship to past climatic events was
always uncertain. The best supporting geomorphic
evidence for an arid Pleistocene was the deltaic deposition
of sands rich in feldspar in sediments of Pleistocene age
near the mout h of the Amazon (Damuth & Fairbridge,
1970). As feldspars degrade under humid conditions, it
was suggested that their presence was further evidence of
Pleistocene aridity (Damuth & Fairbridge, 1970).
Building on the prevailing view of Pleistocene arid-
ity, Wetterberg e t al . (1976) produced an influential
report that prioritized conservation areas using phyto-
geographic areas and, with equal weighting, the
' known' Pleistocene refugia. This report has provided
the foundation for many later assessments of conserva-
tion needs in Amazonia (Rylands, 1991). In 1979, the
Brazilian government adopted the location of proposed
Pleistocene forest refuges as being the mainstay of its
conservation plan (Cgmara, 1983). These areas were
designated if (1) the area was indicated to have been a
Pleistocene refugium for two or more different groups
of organisms; (2) a postulated refugium and unusual or
distinct vegetational formations co-occurred there; and
(3) they were of apparent ecological significance, not
included in the former categories (Cfimara, 1983).
More recently ' Workshop 90' attempted to update
the areas prioritized for conservation. Modern biodi-
versity of a wide range of organisms governed the loca-
tion of proposed conservation areas, although refugial
patterns were also included in the analyses (Fig. 1).
A REAPPRAISAL OF THE REFUGIAL
HYPOTHESIS
The refugial hypothesis was raised on modern biogeo-
graphic distributions of endemic species - - patterns
that have been challenged on methodological grounds
(Nelson e t a l . , 1990). The timescale of the speciation
events that the refugial hypothesis sought to explain
has been challenged (Endler, 1982; Heyer & Maxson,
1982) and alternative hypotheses raised through the
application of cladistic biology (Cracraft & Prum,
1988; Patterson e t a l . , 1992). The geomorphological
data have been re-interpreted and alternative explana-
tions advanced (Milliman & Barretto, 1975: Irion,
1984; Salo, 1987). Furthermore, the refugial argument
has not been supported by radiocarbon-dated paleo-
ecological evidence from Amazonia (Colinvaux, 1987;
Salo, 1987).
Data quality for endemic concentrations
Nelson e t al . (1990) compared the number of plant col-
lections made across Amazonia with the number of
222 M. B. Bus h
Fig. 1. Sketch map of Amazonia showing [] the location of areas postulated with 60-80% confidence to have been Pleistocene
rainforest refugia (Brown, 1987a); ~, areas representing c. 28% of Amazonia, given the top two ranks for conservation prioritiza-
tion, as identified by the 'Workshop 90-Priority areas for Conservation in Amazonia', Manaus, 10-20 January 1990.
II, areas where postulated refugia and conservation zones overlap. With permission from Conservation International.
endemic species recorded for each locality. They found
a correlation between collecting effort and reported
diversity of some families, bearing out the maxim ' if
you look you will find'. Sites along the Amazon River,
e.g. near the major settlements of Manaus, Santar6m,
and Bel6m, and around research bases, appeared from
the biodiversity data to have unusually high concentra-
tions of endemic species, but following the analysis of
Nelson et al. (1990) these appear to be methodological
artifacts. It should be emphasized that not all of the
data for endemic concentrations can be dismissed in
this way, and some local faunas and floras genuinely appear
to have concentrations of endemic species, especially at the
periphery of Amazonia (Nelson et al., 1990; Bush, 1994).
The reappraisal of geomorphic evidence
The geomorphic evidence cited to support refugia has
been contested and reinterpreted by Irion (1984) and
Salo (1987). The stone-lines appear to be either the
leached products of weathering that form pisoliths, or
relictual from the formation of the Belterra Clays
about 2-5 million years ago. The dunes appear to be
pre-Quaternary in age (see Salo (1987) and Colinvaux
(1987) for reviews).
The feldspars in the deltaic deposits of the Amazon
have also been reinterpreted. The alternate explanation
is that the feldspars are reworked materials, eroded
during periods of intense fluvial downcutting in
response to lowered ice-age sea levels (Milliman & Bar-
retto, 1975; Irion, 1984). Thus the refugial argument
may not be able to rely for support on available geo-
morphic evidence.
Paleotemperature: empirical data
Recent papers have described vegetation changes asso-
ciated with ice-age cooling in the lowland neotropics
(Liu & Colinvaux, 1985; Bush & Colinvaux, 1990; Bush
e t a [ . , 1990, 1992; Piperno e t a [ . , 1990; De Oliveira,
1992; Ledru, 1993). Fossil pollen, phytoliths, wood and
diatoms provide evidence of montane vegetational ele-
ments invading the bottomlands. During times of
extreme cooling at c. 33,000 years BP to 30,000 years
BP, and again from 14,000 BP to 12,000 BP a vegeta-
tional descent of about 1500-1800 m is recorded in
Colombia, Ecuador, Brazil and Panama (van der Ham-
men et al. , 1981; Hooghiemstra, 1984; Bush et al. ,
1990; Bush, 1994). Paramo, subparamo and Andean
forest elements shuffled downslope, bringing C3
grasses, Dr i my s , Podcarpus, and Al nus as low as 1000
m elevation in eastern Ecuador. Of particular interest is
the descent of grasses using the C3 photosynthetic
pathway. In tropical South America these grasses are
presently restricted to paramo and subparamo ecosys-
tems, suggesting that they moved about 1500 - 2000 m
vertically downslope. The scale of this descent of vege-
tation is replicated in records from the high Andes to
the interior of lowland Brazil as far south as Minas
Gerais (Hooghiemstra, 1984; Bush e t al . , 1990;
Hooghiemstra & Sarmiento, 1991; De Oliveira, 1992;
Ledru, 1993; Bush, 1994). Such a shift of vegetation
corresponds to about a 7.5 - 9C change in tempera-
ture (assuming a moist air adiabatic lapse rate of 5C
per 1000 m of ascent - - Canadas, 1983; Bush et al. ,
1990; Bush, 1994). These extremely cold temperatures
lasted for several millennia at a time, but for most of
A m a z o n i a n c o n s e r v a t i o n 223
the Pleistocene t he neot r opi cs experi enced a cool i ng of
about 5C relative t o present (Col i nvaux, 1987, 1993;
Bush & Col i nvaux, 1990; Bush, 1994).
These t errest ri al pal eoecol ogi cal dat a appear ed irre-
conci l abl e with sea-surface t emper at ur e est i mat es t hat
i nvoked a cool i ng of j ust IC at 18,000 aP ( CLI MAP,
1976). However , new pal eot emper at ur e evi dence f r om
Car i bbean coral s indicates t hat the sea t emper at ur e
close to land was cool ed by about 5C at 18,000 Bp
( Gui l der son e t al . , 1994). The coral l i ne dat a, based on
r adi omet r i c analysis of gtsO/~60, and rat i os of st ron-
t i um/ cal ci um, are the st rongest oceani c pal eot emper a-
t ure dat a yet obt ai ned f r om the equat or i al region; t hei r
concor dance with the t errest ri al r ecor d is striking.
Paleoprecipitation: empirical and modeled data
Not all pal eoecol ogi cal records f r om l owl and Sout h
Ameri ca show a pur e cool i ng signal. Recor ds f r om the
peri phery of Amazoni a reveal histories of l owered
Pleistocene lake levels. Savanna el ement s are observed
t o have encr oached i nt o what are now t he dri er areas
of Amazoni a (Absy & van der Hammen, 1976; Absy e t
al . , 1991). However , pr onounced dryi ng was brief, rela-
tive t o the overall length of the Pleistocene (van der
Hammen e t al . , 1981; Absy e t al . , 1991), and does not
appear t o have been of sufficient st rengt h t o eradi cat e
rai nforest f r om many areas of Amazoni a. Sites investi-
gat ed in the west ern and nor t hwest er n Amazon reveal
histories of cont i nuous cool moi st forest presence in the
Pleistocene and warm moist forest t hroughout the Holocene
(Liu & Col i nvaux, 1985, 1988; Bush & Col i nvaux, 1988;
Bush e t al . , 1990). It appears t hat the ice-ages were
times of cooling and modest drying in the Amazon basin.
Perhaps the best est i mat e for ice-age dryi ng comes
f r om the cl i mat e model s of Gat es (1976), Manabe and
Hahn (t 977), and Kut zbach and Guet t er (1986) which
suggest a 10-20% reduct i on in preci pi t at i on at 18,000
aP. In an ice-age worl d with at mospher i c CO~ concen-
t rat i ons reduced to 170 ppm (Barnol a e t al . , 1987),
plants are likely to t ranspi re great er amount s of wat er
as t hei r st omat es must remai n open l onger in or der to
accumul at e sufficient CO2 for phot osynt hesi s. Thus the
reduced concent r at i ons of CO, are likely to hei ght en
dr ought stress. Bush (1994) suggests, t herefore, t hat the
larger of the model ed preci pi t at i on reduct i ons be
accept ed as most closely appr oxi mat i ng t he effective
dr ought stress experi enced by Amazoni an plants.
The preci pi t at i on map of Amazoni a can be r edr awn
(Fig. 2) to accommodat e this 20% r educt i on in rainfall,
and t o show the areas of overl appi ng endemi sm for
birds, plants and butterflies (Brown, 1987). This model
of a 20% reduct i on in preci pi t at i on accommodat es the
observed veget at i on changes in every pal eoecol ogi cal
dat um f r om the neot ropi cal regi on (Bush, 1994). Paleo-
ecological records t hat show pr onounced Pleistocene
dryi ng are seen to lie in regions suppor t i ng less t han
2000 mm of rain, and t herefore were ecot onal areas
t hat may have suppor t ed forest, cerrado, or savanna, at
vari ous times duri ng the ice-age. Areas receiving mor e
t han 2000 mm of rain are likely to mai nt ai n a forest
(albeit with a novel assor t ment of l owl and species). In
these areas t hat were per manent l y wet the pal eoecol ogi -
cal dat a show the cont i nuous presence of moi st
forest. In receiving less t han 1500 mm the veget at i on
woul d have been a cl osed-canopy dry forest, cer r ado oz"
savanna, accordi ng to local edaphi c condi t i ons or
Fig. 2. Sketch map of Amazonia showing the location of paleoecological sites, and whether they indicate the expansion of non-
forest elements, relative to a modeled 20% reduction in precipitation during the last glacial cycle (after Bush, 1994). U, area pos-
tulated to receive >2000 mm precipitation with 20% drying; [~, area postulated to receive 2000-1500 mm precipitation with 20%
drying; 1--], area postulated to receive <1500 mm precipitation with 20% drying; ~ , paleological datum indicating drying (and
consistent with cooling); , paleological datum indicating cool, moist conditions.
224 M. B. Bush
fire regimes. At precipitation levels close to 1500 mm
per annum there is an increased likelihood of the lake
dryi ng out completely, either t hr ough evaporative loss
or t hr ough the lowering of the water table. Lakes t hat
lie in the region receiving <1500 mm rainfall per annum
often show prot ract ed dr y periods in the late Plei-
stocene, or onl y started to hol d wat er with the rise of
Hol ocene wat er tables.
I f these preci pi t at i on dat a are compar ed with the
post ul at ed centers of endemi sm (Brown, 1987), it is evi-
dent t hat the loci of endemic richness lie at the edge of
the moi st ice-age forests, not at their center (Fig. 3).
This pat t ern is inconsistent wi t h the refugial hypot he-
sis, as endemi sm appears to reflect those areas most
likely to be subject to envi ronment al change, rat her
t han those likely to have a const ant envi ronment . The
' refugia' lie in areas most likely to be invaded by mon-
t ane t axa surging down the flank of the Andes, or in
ecot onal areas where small changes in precipitation
result in savanna expansi on duri ng dry phases and the
mai nt enance of rai nforest duri ng wetter ones.
The cool i ng hypot hes i s vs t he refugi al hypot hes i s
The empirical dat a deny the possibility t hat Amazoni an
hilltops had t emperat ures within 2C of present and
t hat these areas coul d have support ed an unchanged
flora t hr oughout the nor t her n hemispheric glacial max-
ima. Indeed, the hilltops shoul d be seen as the areas
most likely to change as t hey woul d have been t oo cold
for many l owl and rai nforest t axa to persist. Amazoni a
was not warm and arid at the last glacial maxi mum as
suggested by the refugialists, but cold and slightly drier
t han present.
The critical poi nt to appreciate from these two differ-
ent account s is not the act ual speciation mechanism,
but the implied envi ronment al differences in the
endemic-rich regions relative to the core of Amazoni a
and the ecological stability, or lack of it, of isolated
patches of forest. In the refugial account of events, the
forest isolates are purport ed to have survived as wet
areas in an overall dry landscape. Accordi ng to the new
paleoclimatic evidence, the Pleistocene was not warm
and arid, but cool, and the rainforest was not broken
up into isolates. Duri ng the Pleistocene the moder n
centers of endemi sm were often relatively dry areas (or
areas invaded by col d-adapt ed Andean plants) lying at
the periphery of a vast moist forest block. The center
and western port i on of the Amazon basin were not
savanna but moist forest moderat i ng climatic change.
I MPLI CATI ONS OF A REVI SED SPECI ATI ON
MODEL FOR CONSERVATI ON BI OLOGY
Prioritization of conservat i on areas has been based on
moder n biogeographic areas of high biodiversity
(Ryl ands, 1991). For these areas to be valuable
reserves, it is necessary to predict how t hey will be
affected by devel opment elsewhere in Amazoni a. The
' refugial hypot hesi s' has pl ayed a vital part in formu-
lating a conservat i on strategy for Amazoni a. This
hypot hesi s was valuable in i nt roduci ng a t emporal ele-
ment to the debat e over conservation, but it may have
provi ded a false sense of ecosystem stability for por-
tions of the Amazon basin. Worse, it may have sug-
gested t hat areas of high biodiversity could, unchanged,
wi t hst and landscape al t erat i on in the surroundi ng
region. Because many of the areas of high biodiversity
were t hought to have been refugia, it was assumed t hat
Fig. 3. Sketch map showing the location of endemic centers relative to precipitation assuming a 20% effective drying during
glacial times. Endemic centers lie either in the marginal forest areas or within the range of migration of the Andean flora (after
Bush, 1994). i , overlap of areas of bird, butterfly and plant endemic richness; ~, overlap of two areas of bird, butterfly, or plant
endemic richness; I~, subtropical vegetation. Estimated precipitation: 17~, >2000 ram; R, 2000-1500 mm; I-7, <1500 mm.
Amaz oni an conservat i on 225
t hey survived in isolation for t housands of years duri ng
glacial conditions. As one of the predictions of environ-
ment al change wr ought by deforest at i on of Amazoni a
is increasing aridity, the refugial hypot hesi s offers the
hope t hat these prioritized conservat i on areas woul d be
well located to survive drying, j ust as t hey did in the
Pleistocene. However, the falsification of the climatic
assumpt i ons of the refugial hypot hesi s leads to the need
to reassess conservat i on strategies based on t hat model.
The endemic-rich areas can be divided into two basic
categories: those t hat have very high rainfall (>3000
ram), and those t hat , given a 20% drying, become eco-
tonal between moist forest and cerrado. The wettest
sites are primarily the ones al ong the Andean flank,
and these will be sensitive to changes in t emperat ure,
part i cul arl y cooling, but may be relatively insensitive to
changes in precipitation. Cont rast i ngl y, the ecot onal
areas, far from being areas capable of surviving the
buffets of increasing aridity, are most sensitive to cli-
mat i c change. They were not separated by savanna
duri ng ice-age time, but lay at the margi n of a massive
forest block t hat still received more t han 2000 mm of
rain, with high evapot ranspi rat i on rates helping to
mai nt ai n a moi st ure-l aden envi ronment . The forest
would have moder at ed some of the effects of drying,
and would have offered a wetter retreat for some
species duri ng times of exceptional drought . Thus the
ecot onal areas, identified as areas of exceptionally high
biodiversity, cannot st and alone. To predicate conser-
vat i on strategies based on their existence as isolates is
unwise.
Reliance on small islands of veget at i on for conserva-
tion will lead to the reduct i on of bot h faunal and floral
diversity, especially as these areas come under the pres-
sure of climatic change. Estimates of mi ni mum sized
areas to protect popul at i ons, e.g. the 250,000 ha reserve
size (Terborgh, 1974; Myers, 1979; Higgs & Usher,
1980), are onl y appropri at e so long as the regional cli-
mat e remains const ant (Peters & Darling, 1985).
Reserves of this size may be large enough to mai nt ai n
breeding popul at i ons of most organisms under steady-
state conditions, but t hey are t oo small to be self-regu-
lating climatic units in an increasingly arid landscape
(Peters & Darling, 1985; Peters, 1998).
Rat her t han choosi ng conservat i on areas for endemic
richness alone, it would be better to preserve enough of
the core Amazoni an forest to mitigate local climatic
change, and to concent rat e on the areas t hat are likely
to stay moi st enough, given the scale of deforest at i on,
to support tropical forest. This may mean t aki ng a sec-
tion of the ecot onal area and a port i on of the adj acent
forest, so t hat i f the climate becomes drier, species can
migrate into a wetter area.
Ot her climatic changes may drive species to migrate
between elevations. At the edge of massifs, species will
respond to local or global t emperat ure changes by
mi grat i ng up or down mount ai n sides, e.g. the Andes,
the Gui anan Shield or the At l ant i c coastal mount ai ns.
At present it is easiest to envisage a warmi ng trend t hat
woul d lead to an upslope mi grat i on of taxa, but a
renewed stadial, such as the little ice-age of c. 1400 -
1800 AD, could at some poi nt result in the descent of
vegetation types. It is essential, therefore, t hat parks
allow fut ure mi grat i on of t axa in response to climatic
change. Ideally protected lands would form belts rang-
ing from the highest peak down into the lowlands. In
Ecuador, such a park has already been established, e.g.
the 270,000 ha Sangay Nat i onal Park t hat extends from
5000 m elevation down to 800 m elevation (Anhalzer,
1988). Anot her example is the Brazilian Pico da
Neblina reserve, close to the Venezuelan border, t hat
includes an elevational range from 3000 m down to
about 100 m above sea level.
DEVELOPMENT OF NON- RESERVE LANDS
Preserving Amazoni an biodiversity is not simply a mat-
ter of identifying conservat i on areas. These nat i onal
parks will not funct i on in isolation, and it is critical
t hat the intervening areas are developed in such a way
t hat the moi st ure cycles of the Amazoni an climate are
mai nt ai ned. Not all of the core forests of Amazoni a
have to be set aside as unt ouched wilderness areas, but
their devel opment shoul d protect t hem from reduct i on
to pasture. No studies are available detailing the long-
term moi st ure flux from sustainable silviculture or
agroforestry, but climate models indicate t hat t hey
would provide a surface t hat more closely resembles
nat ural forest t han woul d pasture (Shukla et al., 1990).
Sustainable silviculture, mixed perennial polycultures
or i nt erpl ant i ng of crops with economically i mport ant
trees may all be appropri at e land uses t hat woul d pro-
vide an income while minimizing local climatic change.
The rights of indigenous peoples have come to the
forefront of the conservat i on debate, and present plan-
ners with a difficulty. Their right to a nat i onal home-
l and is undeniable, and the designation of areas as
protected ' Indi an lands' may preserve large tracts of
forest, but this relies on the indigenous people choosing
to mai nt ai n forest on their land. As the control of these
lands is passed to the indigenous popul at i on, no guar-
antee exists as to their fut ure use (Eden, 1990). Fur-
thermore, it is possible t hat their goals, even their
vision of what constitutes sustainability, do not mat ch
those of the conservationists (Redford & Macl ean
Stearman, 1993). The hope is t hat the t radi t i onal ways
of hunt i ng and harvesting would mai nt ai n the forest,
but there is increasing evidence of those t radi t i ons
being abandoned in favor of ' progress' (Redford &
Macl ean Stearman, 1993).
About 60% of present forest destruction in Amazo-
nia can be at t ri but ed to sl ash-and-burn cultivation, a
non-sust ai nabl e cycle of l and use t hat leads to erosion,
falling crop yields and furt her forest destruction
(Jacobs, 1981). Clearly a complete conservat i on policy
for Amazoni a should include an educat i onal element
226 M. B. Bu s h
t hat pr omot es t he sust ai nabl e devel opment of t he land,
and this includes t he pr omot i on of these ideals with t he
new generat i ons of i ndi genous peoples. Fur t her mor e,
any concept of sust ai nabi l i t y must include not onl y t he
harvest i ng of t he land, but also t he mai nt enance of the
local climate. I f t he interstices bet ween conser vat i on
areas are degraded, the par ks themselves will surely
fail.
CONCLUSI ONS
Preservi ng endemi c species and maxi mal bi odi versi t y
must be an essential pl ank of Amazoni an conser vat i on
strategies, and this means pri ori t i zi ng areas with high
species concent rat i ons. However , given f ut ur e climatic
change, pr ot ect i ng these areas al one will not pr ovi de a
successful conser vat i on policy. A conf i gur at i on of
reserves wi t hout t aki ng i nt o account t he likely effects of
f ut ur e cl i mat e change may lead t o severe management
pr obl ems in the fut ure. The assumpt i on t hat areas of
high moder n bi odi versi t y are stable dur i ng times of cli-
mat i c change, as suggested by t he refugial hypot hesi s,
is i nconsi st ent with empirical pal eoecol ogi cal evidence.
Far f r om bei ng stable ' refugi a' , these areas appear t o
have been the ecot onal edge of t he Pleistocene rain-
forests. I f Amazoni an devel opment results in decreased
evapot r anspi r at i on and reduced preci pi t at i on, these
areas will once agai n be ecot onal , but this t i me wi t hout
the core of moi st forest, and t hei r species subject to
enhanced l i kel i hood of ext i nct i on. Conser vat i on initia-
tives di rect ed t o mai nt ai ni ng maxi mal bi odi versi t y
shoul d allow f or the mi gr at i on of species in t he face of
f ut ur e cl i mat e change. Such change may be mani fest ed
as a cool i ng or a war mi ng in associ at i on with dryi ng,
and reserves shoul d be established with as much eleva-
t i onal and moi st ur e range as possible. ' Ret r eat areas' ,
where species can mi grat e duri ng times of change,
shoul d be i ncor por at ed i nt o t he est abl i shment of
reserve areas. Reserves shoul d be ar r anged so as t o
pr ovi de large cont i nuous bl ocks of veget at i on cont ai n-
ing a full range of nat ur al habi t at s. It is unlikely t hat
all of t he sites present l y identified as being of excep-
t i onal biological interest can be i ncor por at ed i nt o such
large t ract s of reserve land. Such pr agmat i c decisions
will lead t o t he sacrifice of some areas of high bi odi ver-
sity so t hat some ver y large reserves can be mai nt ai ned.
Even with this trade-off, less bi odi versi t y woul d be lost
t han wi t hi n undersi zed island reserves dur i ng times of
climate change.
In the near fut ure, t he local cl i mat e of Amazoni a is
likely t o become war mer and dri er as a result of defor-
estation. The result will be envi r onment s wi t hout past
anal og. The climatic di vergence and hence t he vegeta-
t i on change will become mor e ext reme a s increasing
areas of t he core forest are conver t ed to pasture. In
or der to mai nt ai n areas present l y rich in endemi c
species, it is essential t hat t he devel opment of cent ral
Amazoni a, an area generally consi dered t o be poor in
these species, be done in such a way t hat present
climatic condi t i ons are mai nt ai ned. Areas bet ween the
conservat i on areas, wherever possible, shoul d be t reat ed
as buffer zones in which l and management , i f not actu-
ally pr omot i ng conservat i on, is not prejudicial to its
success ( s ens u Saunders e t al . , 1991). It is recom-
mended, t herefore, t hat management pl ans pri ori t i ze
central Amazoni a as a zone of regulated land use centered
on sust ai nabl e silviculture or agroforest ry, or (with the
reservat i ons not ed above) f or use as ' I ndi an lands' .
ACKNOWLEDGEMENTS
My t hanks t o Dani el Livingstone. Paul o De Oliveira,
Geor ge De Busk, Adr i enne Pilmanis, Renat o Ci nt ra
and Pet er Ji pp f or comment s on the manuscri pt . Paul
Col i nvaux and his research t eam were integral to gath-
ering t he dat a f or t he pal eoecol ogi cal dat a present ed
and f or many st i mul at i ng debates. The pal eoecol ogi cal
wor k was funded by NSF grant s ATM 8709685, BSR
9007019 and SES-881110.
REFERENCES
Ab'Sfiber, A. N. (1982) Paleoclimate and paleoecology of
Brazilian Amazonia. In Biological diversification in the trop-
ics, ed. G. T. Prance. Columbia University Press, New
York, pp. 41-59.
Absy, M. L., Cleef, A, Fournier, M. et al., (1991). Mise en
6vidence de quatre phases d' ouverture de la for~t dense
dans le sud-est de L'Amazonie au cours des 60,000
derni6res ann6es. Premiere comparaison avec d'autres
regions tropicales. C. R. Acad. Sci. Paris, Series II, 312,
673-8.
Absy, M. L. & van der Hammen, T. (1976). Some palaeoeco-
logical data from Rond6nia, southern part of the Amazon
Basin. Act. Amazon. , 6, 293-9.
Anhalzer, J. (1988). Sangay Parque nacional. Azuca, Quito.
Barnola, J. M., Raynaud, D., Korotkevitch, Y. S. &
Lorius, C. (1987). Vostoc ice core provides 160,000 year
record of atmospheric CO 2. Nature, Lond. , 329, 408-14.
Brown, K. S. Jr (1982). Paleoecological and regional patterns
of evolution in neotropical forest butterflies. In Biological
diversification in the tropics, ed. G. T. Prance. Columbia
University Press, New York, pp, 25-308.
Brown, K. S. Jr (1987). Biogeography and evolution of
neotropical butterflies. In Biogeography and quaternary his-
tory in tropical America, ed. T. C. Whitmore & G, T.
Prance. Oxford Science Publications, Oxford, pp. 66-104.
Bush, M. B. (1994). Amazonian speciation: a necessarily
complex model. J. Biogeogr., 21, 5-17.
Bush, M. B. & Colinvaux, P. A. (1988). A 7000-year pollen
record from the Amazon lowlands, Ecuador. Vegetatio, 76,
141-54.
Bush, M. B. & Colinvaux, P. A. (1990). A long climatic and
vegetation record from lowland Panama. J. Veget. Sci,, 1,
105-18.
Bush, M. B., Colinvaux, P. A., Wiemann, M. C., Piperno, D. R.
& Liu, K.-b. (1990). Pleistocene temperature depression
and vegetation change in Ecuadorian Amazonia. Quat.
Res., 34, 330-45.
Bush, M. B., Piperno, D. R., Colinvaux, P. A., De Oliveira,
P. E., Krissek, L. A., Miller, M. C. & Rowe, W. E. (1992).
A 14,300 year paleoecological profile of a lowland tropical
lake in Panama. EcoL Monogr. , 62, 251-75.
A ma z o n i a n c o n s e r v a t i o n 227
C/tmara, I de G. (1983), Tropical moist forest conservation in
Brazil. In Tropical rain f or e s t ecology and management , ed.
S. L. Sutton, T. C. Whi t more & A. C. Chadwick. Black-
well Scientific Publications, Oxford, pp. 413-21.
Camargo, J. M. F. (1978). O grupo Part amona ( Par t amona)
testacea (Klug); suas especies, distribuicao e differenciacao
geografica (Meliponinae, Apidae, Hymenoptera). Act a
Amaz . , 10 (suppl.), 1-175.
Canadas, L. C. (1983). El mapa biocliomatico y ecologico del
Ecuador. Ministerio Agricultura Pronareg, Quito.
CLI MAP Project Members (1976). The surface of the ice-age
Earth. Science, N. Y., 191, 1131-7.
Colinvaux, P. A. (1987). Amazon diversity in the light of the
paleoecological record. Quat. Sci. Rev. , 6, 93-114.
Colinvaux, P. A. (1993). Pleistocene bi ogeography and diver-
sity in tropical forests of Sout h America. In Biological rela-
tionships between Af ri ca and Sout h Ameri ca, ed. P.
Goldblatt. Yale University Press, New Haven, CT, pp. 473-99.
Cracraft, J. & Prum, R. O. (1988). Patterns and processes of
diversification: speciation and historical congruence in
some neotropical birds. Evolution, 42, 603-20.
Damut h, J. E. & Fairbridge, R. W. (1970). Equatorial
Atlantic deep-sea arkosic sands and ice-age aridity in tropi-
cal South America. Bull. Geol. Soc. Amer. , 81, 189-206.
De Oliveira, P. E. (1992). A palynological record of late
Quat ernary vegetational and climatic change in southeast-
ern Brazil. PhD thesis, Ohi o State University, Columbus,
OH.
Di amond, J. M. (1976). Island bi ogeography and conserva-
tion: strategy and limitations. Science, N. K, 193, 1027-9.
Dickinson, R. E. (1991). A comment ary on: probabl e impact
of deforestation on hydrological processes. Climatic
Change, 19. 175.
Dub& Y. (1980). Em busca de uma politica florestal para a
Amaz6ni a brasiliera. Superintend~ncia do Desenvolvi-
ment o da Amaz6ni a, Beldm.
Duellman, W. E. (1972). South America frogs of the I t y l a
rostrata group (Amphibia, Anura, Hylidae). Zool. Meded. ,
47, 177 92.
Duellman, W. E. (1982). Quat ernary climatic-ecological fluc-
tuations in the lowland tropics: frogs and forest. In Biologi-
cal diversification in the tropics, ed. G. T. Prance. Col umbi a
University Press, New York, pp. 389402.
Eden, M. J. (1990). Ecology and land management in Amaz o-
nia. Belhaven Press, London.
Endler, J. A. (1982). Pleistocene forest refuges: fact or fancy?
In Biological diversification in the tropics, ed. G. T. Prance.
Col umbi a University Press, New York, pp. 641-57.
Fearnside, P. M. & Ferreira, G. de L. (1984). Roads in
Rond6ni a: highway const ruct i on and the farce of unpro-
tected forest reserves in Brazil' s Amazon forest. Environ.
Conserv., 11, 358-60.
Gates, W. L. (1976). Modeling the ice-age climate. Science,
N. K, 191, 1138-44.
Ginsburg, J. R. (1987). What is conservation biology? Trends'
Ecol. & Evolut., 2, 2624.
Goodl and, R. J. A. & Irwin, H. S. (1975). Amaz on j ungl e:
green hell to red desert? Elsevier Scientific Publishing,
Amsterdam.
Guilderson, T. P., Fairbanks, R. G. & Rubenstone, J. L.
(1994). Tropical temperature variations since 20,000 years
ago: modul at i ng interhemispheric climate change. Science,
N. Y., 263, 663 5.
Haffer, J. (1969). Speciation in Amazoni an forest birds. Sci-
ence, N. Y. , 165, 131 7.
Heyer, W. R. & Maxson, L. R. (1982). Distributions, rela-
tionships, and zoogeography of lowland frogs. In Biologi-
cal diversification in the tropics, ed. G. T. Prance. Col umbi a
University Press, New York, pp. 375 88.
Higgs, A. J. & Usher, M. B. (1980). Should nature reserves
be large or small? Nat ure, Lond. , 285, 568-9.
Hooghiemstra, H. (1984). Vegetational and climatic hi st ory oJ
the high plain o f Bogota, Colombia: a continuous record o f
the last 3 5 million years. Gant ner Verlag, Vaduz.
Hooghiemstra, H. & Sarmiento, G. (1991). Long continental
pollen record from a tropical intermontane basin: late
Pliocene and Pleistocene history from a 540-meter core.
Episodes, 14, 107-15.
Irion, G. (1984). Sedimentation and sediments of Amazoni an
rivers and evolution of the Amazoni an landscape since
Pliocene times. The Amazon. Li mnol ogy and landseape o f a
might)' tropical river and its basin, ed. J. Sioli. Dr W. Junk,
Dordrecht, pp. 2014.
Jacobs, M. (1981). An introduction to tropical Jorests.
Springer Verlag, Hamburg.
Journaux, A. (1975) Recherches geomorphologiques en Ama-
zonie Bresilienne. Bull. Centre Geomorph. Caen ( CNR S ) ,
20, 1-67.
Kutzbach, J. E. & Guetter, P. J. (1986). The influence of
changing orbital parameters and surface boundar y condi-
tions on climate simulation for the past 18,000 years. J.
Atrnos. Sci. , 43, 1726-59.
Lean, J. & Warrilow, D. A. (1989). Simulation of the
regional climatic impact of Amazoni an deforestation.
Nat ure, Lond. , 342, 411-13.
Ledru, M.-P. (1993). Late Quat ernary environmental and
climatic changes in Central Brazil. Quat. Res. , 39, 90-8.
Liu, K.-b. & Colinvaux, P. A. (1985). Forest changes in the
Amazon basin during the last glacial maximum. Nature,
Lond. , 318, 556-7.
Liu, K.-b. & Colinvaux, P. A. (1988). A 5200-year history of
Amazon rain forest. J. Biogeogr., 15, 23148.
Lourenco, W. R. & Florez, E. (1991). Scorpions (Chelicerata)
from Colombia: Il I. The scorpion thuna of Pacific region
(Choco), with some biogeographic considerations. Amazo-
niana, 1| , 119-34.
Lovejoy, T. E., Bierregaard, R. O. Jr, Rylands, A. B., Mal-
colm, J. R., Quintela, C. E., Harper, L. H., Brown, K. S. Jr,
Powell, A. H., Powell, G. V. N., Schubart, O, R. & Hays, M.
(1986). Edge effects and other effects of isolation on
Amazoni an forest fragments. Conserv. Biol. ed. M. Soule.
Sinauer Assoc. Inc. Sunderland, MA. pp. 257 85.
MacArt hur, R. H. & Wilson, E. O. (1967). The theory o["
island biogeography. Princeton Press, Princeton, NJ.
McNeely, J. A. (1992). The biodiversity crisis: challenges for
research and management. In Conservation o f biodiversity
f o r sustainable development, ed. O. T. Sandlund, K. Hi ndar
& A. H. D. Brown. Scandinavian University Press, Oslo,
pp. 15-26.
Manabe, S. & Hahn, D. G. (1977). Simulation of the tropical
climate of an ice-age. J. Geophys. Res. , 82, 3889-911.
Milliman, J. D & Barretto, H. T. (1975) Relict magnesium cal-
cite oolite and subsidence of the Amazon shelf. Sedi ment ol -
ogy, 22, 13745.
Myers, N. (1979). The sinking ark. A new look at the probl em
o f disappearing species. Pergamon Press, Oxford.
Myers, N. (1984). The pri mary source. Tropical j or e s t s and
our f ut ure. W. W. Nort on, New York.
Myers, N. (1988). Tropical forests and their species: going,
going...? In Biodiversity, ed. E. O. Wilson & F. M. Peter.
National Academy Press, Washington, DC, pp. 28 35.
Nelson, B. W., Ferreira, C. A. C., da Silva, M. F. &
Kawasaki, M. L. (1990). Endemism centres, refugia and
botanical collection density in Brazilian Amazonia. Nature,
Lond. , 345, 714-16.
Odum, E. P. & Odum, H. T. (1972). Nat ural areas as neces-
sary component s of man' s total environment. Trans. NA
Wildl. Nat. Resour. Conj., 37th, Mexico City, pp. 178 89.
228 M. B. Bu s h
Pandolfo, C. (1974). Est udi os basieos para o est abel eci ment o
de uma politica de desenvolvimento dos recursos f l orest ai s e
de uso racional das terras da Amaz6ni a, 2nd edn. Superin-
tend~ncia do Desenvolvimento da Amaz6nia, Bel6m.
Patterson, B. D., Pacheco, V. & Ashley, M. V. (1992). On the
origins of the western slope region of endemism: systematics
of fig-eating bats, genus Artibeus. Me m. Mus. Hist. Nat . ,
UNMSM, 21, 189-205.
Peters II, R. L. (1988). The effect of global climatic change
on natural communities. In Biodiversity, ed. E. O. Wilson.
National Academy Press, Washington, DC, pp. 450-61.
Peters, II, R. L. & Darling, D. J. S. (1985). The greenhouse
effect and nature reserves: global warming would diminish
biological diversity by causing extinctions among reserve
species. Bi oSei ence, 35, 707-17.
Piperno, D. R., Bush, M. B. & Colinvaux, P. A. (1990). Paleo-
environments and human settlement in late-glacial
Panama. Quat. Res. , 33, 108-16.
Pitman, A. J., Durbidge, T. B. & Henderson-Sellers, A.
(1993). Assessing climate model sensitivity to prescribed
deforested landscapes. Int. J. Climatol., 13, 879-98.
Prance, G. T. (1982). Forest refuges evidence from woody
angiosperms. In Biological diversification in the tropics, ed.
G. T. Prance. Columbia University Press, New York, pp.
137-56.
Prance, G. T. (1987). Biogeography of neotropical plants. In
Biogeography and Quat ernary hi st ory in tropical Ameri ca,
ed. T. C. Whitmore & G. T. Prance. Oxford Science Publi-
cations, Oxford, pp. 46-65.
Redford, K. H. & Maclean Stearman, A. (1993). Forest
dwelling native amazonians and the conservation of biodi-
versity: interests in common or in collision? Conserv. Biol.,
7, 248-55.
Richards, P. W. (1952). The tropical rain f orest . An ecological
study. Cambridge University Press, Cambridge.
Rylands, A. B. (1991). The st at us o f conservation areas in the
Brazilian Amazon. World Wildlife Fund, Washington, DC.
S~etersdal, M., Line, J. M. & Birks, H. J. B. (1993). How to
maximize biological diversity in nature reserve selection:
vascular plants and breeding birds in deciduous wood-
lands, western Norway. Biol. Conserv., 66, 131-8.
Salati, E. & Nobre, C. A. (1991). Possible climatic impacts of
tropical deforestation. Climatic Change, 19, 177-96.
Salati, E., Dall'Olio, A., Matsui, E. & Gat, J. R. (1979).
Recycling of water in the Amazon basin: an isotopic study.
Wat er Resour. Res. , 15, 1250-8.
Salo, J. (1987). Pleistocene forest refuges in the Amazon:
evaluation of the biostratigraphical, lithostratigraphical
and geomorphological data. Annal. Zool. Fenn., 24, 203-11.
Saunders, D. A., Hobbs, R. J. & Margules, C. R. (1991). Bio-
logical consequences of ecosystem fragmentation: a review.
Conserv. Biol., 5, 18-32.
Shafer, C. L. (1990). Nat ure reserves. Isl and t heory and
conservation practice. Smithsonian Institution Press, Wash-
ington, DC.
Shukla, J., Nobre, C. & Sellers, P. (1990). Amazon deforesta-
tion and climate change. Science, N. E, 247, 1322-6.
Simberloff, D. S. & Abele, L. G. (1976). Island biogeography
theory and conservation practice. Seience, N. Y., 191, 285-6.
Skole, D. & Tucker, C. (1993). Tropical deforestation and
habitat fragmentation in the Amazon: satellite data from
1978 to 1988. Science, N. Y., 260, 1905-10.
Terborgh, J. (1974). Preservation of natural diversity: the
problem of extinction prone species. BioScience, 24,
715-22.
Terborgh, J. (1976). Island biogeography and conservation:
strategy and limitations. Science, N. Y., 193, 1029-30.
Terborgh, J. & Winter B. (1980). Some causes of extinction.
In Conservation biology." an evol ut i onary-ecol ogi cal perspec-
tive, ed. M. E. Soul6 & B. A Wilcox. Sinauer Associates,
Sunderland, MA, pp. 119-33.
Tricart, J. (1974). Existence au Quaternaire de p6riodes
s6ches en Amazonie et dans les r6gions voisines. Rev. Geo-
morph. Dynam. , 223 145-58.
van der Hammen, T., Barelds, J., De Jong, H. & De Veer,
A. A. (1981). Glacial sequence and environmental history
in the Sierra Nevada del Cocuy (Colombia). Palaeogeogr.,
Palaeoclim. , Palaeoecol., 32, 247-340.
Vanzolini, P. E. (1970). Zoologia sistematica, geografia e a
origem das especies. Inst. Geogr. S~o Paulo, Seri e Teses e
Monogr. , 3, 1-56.
Vanzolini, P. E. & Williams, E. E. (1981). The vanishing
refuge: a mechanism for ecogeographic speciation. Pap.
Avul sos Zool. ( $6o Paul o) , 34, 251-5.
Western, D. (1992). The biodiversity crisis: a challenge for
biology. Oi kos, 63, 29-38.
Wetterberg, G. B., Padua, M. T. J., de Castro, C. S. & de
Vascocellos, J. M. C.,(1976). Uma analise de prioridades
em conservacao da natureza. Proj et o de Desenvol vi ment o e
pesquisa f l orest al ( P R ODE P E F ) PNUD/ FAO/ I BDF/ BRA-
45, Seri e Tecnica, 8.
Willis, E. O. (1974). Populations and local extinctions of
birds on Barro Colorado Island, Panama. Ecol. Monogr. ,
44, 153-69.
Willis, E. O. (1979). The composition of avian communities
in remanescent woodlots in southern Brazil. Pap. Avul sos
Zool. ( Sdo Paul o) , 33, 1-25.
Wilson, E. O. (1992). The diversity o f life. Norton, New York.