Amazonian and neotropical plant communities on glacial time-scales

29 Pages·1999·1.13 MB·English

QuaternaryScienceReviews19(2000)141}169
Amazonian and neotropical plant communities on glacial time-scales:
The failure of the aridity and refuge hypotheses
P.A. Colinvaux(cid:1)(cid:2)*(cid:2)(cid:1), P.E. De Oliveira(cid:2)(cid:2)(cid:3), M.B. Bush(cid:4)
(cid:1)SmithsonianTropicalResearchInstitute,Panama
(cid:2)DepartmentofPaleontologyandStratigraphy-DPE,InstitutodeGeociencias-UniversidadedeSaJoPaulo,CaixaPostal11340,SP05422-970,Brazil
(cid:3)FieldMuseumofNaturalHistory,Chicago,IL,USA
(cid:4)DepartmentofBiologicalSciences,FloridaInstituteofTechnology,Melbourne,FL,32901USA
Abstract
PlantsrespondtoPleistoceneclimaticchangeasspecies,notasassociationsorbiomes.Thishasbeendemonstratedunequivocally
by paleobotanical data for temperate latitudes. In the far richer vegetations of the tropics species populations also #uctuated
independentlyinresponsetoclimaticforcing,fromtheirlonglastingglacialstatestothepatternsofbriefinterglacialslikethepresent
andbackagain.WeusepollendatatoreconstructthevegetationoftheAmazonbasininoxygenisotopestages3and2ofthelast
glaciation in order to measure how the plant populations of the Amazon responded to the global warming at the onset of the
Holocene.We"ndthatplantcommunitiesoftheneotropicsventcopiouspollentolakesedimentsandthatthispollenyieldspowerful
signalsfor communitycomposition.Threecontinuoussedimentaryrecordsreachingthroughoxygen isotopestage 2are available
fromtheAmazonlowlands,thosefromCarajas,LakePataandmarinedepositso!themouthoftheAmazonRiver.Allthreerecords
yieldpollenhistoriesofremarkableconstancyandstability.Bycomparingthemwithdepositsofequalantiquityfromthecerrado
(savanna)ofcentralBrazil,weshowthatmostoftheAmazonlowlandsremainedunderforestthroughoutaglacialcycle.Thisforest
wasneverfragmentedbyopenvegetationaspostulatedbytherefugiahypothesis.Insteadtheintactforestofglacialtimesincluded
signi"cantpopulations of plants that are now montane,suggesting that theglobal warmingof the early Holocene resulted in the
expulsionof heat intolerantplantsfrom thelowlandforest.Pollendatafrom theAmazonian#ankof the AndesandfromPaci"c
Panamaprovideevidencethatpopulationsoftheseheatintolerantplantssurvivetheheatofinterglacialsinpartbymaintaininglarge
populationsatcoolermontanealtitudes.OurconclusionthattheAmazonlowlandswereforestedinglacialtimesspeci"callyrefutes
thehypothesisofAmazonianglacialaridity.Accordinglyweexaminethegeomorphologicalevidenceforglacialaridityand"ndit
wanting.OfthethreepaleodunesystemsreportedfortropicalSouthAmerica,thatofNEBrazilwasactiveintheHoloceneaswellas
thePleistocene.PartsofNEBrazilwereactuallymoisterthannowinlate-glacialtimes.PaleodunesinthePantanalhaveneverbeen
seenonthe ground,andthoseintheOrinocoLlanosareundatedandmaybeofanyagesincetheTertiary. Arkosicsandsinthe
Amazon fan deposits came from the Andean foothills or from down cutting by rivers and cannot be evidence of a former arid
land surface. White sands of Amazonia formed as podzols, not by aeolian activity. Such Amazonianstone lines as have received
critical scrutiny are concretionary pisolites in stratigraphic formations that are more than ten million years old. Although the
Amazonwasneverarid,modelingcoolerglacialtropicsgivesplausibilitytoa somewhatdrier Amazoninglacialtimes,aconcept
givensubstancebypollendataforthemovementofecotonesinRondonia,bystreamhistoriesintheBolivianAndes,andbyevidence
for lowered lake levels at Carajas and Lake Pata. But this reduced precipitation was never enough to fragment the forest in the
Amazonlowlandsthemselves.PleistocenemammalsoftheNaporivervalleyinEcuadorwereabletolivealongtheriversystemin
aforestedlandscape.Ourdatasuggestthatthe Amazonforests havebeenstablesincethe startof thePleistocene,afact thathas
contributedtothestorageofvastdiversity.ThecominganthropogenicglobalwarmingandCO enrichmentwilladdtotheglobal
(cid:3)
warmingalreadyenduredbyAmazonbiotaintheHolocene.Wethinkitpossiblethattheexpulsionfromthelowlandforestsofheat
intolerantspeciesis alreadycompleteandthattheforestpropertyofmaintainingitsown microhabitatwillallowthehighspecies
richness to survive more global warming, provided large enough tracts of forest are preserved. (cid:1) 1999 Elsevier Science Ltd. All
rightsreserved.
*Correspondingauthor. (cid:1)Present address: Marine Biological Laboratory, 7 MBL Street,
E-mail addresses: [email protected] (P.A. Colinvaux), WoodsHole,MA02543,USA
[email protected](P.E.DeOliveira),mbush@"t.edu(M.B.Bush)
0277-3791/99/$-seefrontmatter (cid:1) 1999ElsevierScienceLtd.Allrightsreserved.
PII: S0277-3791(99)00059-1
142 P.A.Colinvauxetal./QuaternaryScienceReviews19(2000)141}169
1. Introduction (Nimer, 1989). By far the greater part of the lowlands
below 1000m elevation are forested at present, though
Thisisanecologicalenquiry.Weexaminetheresponse with a great diversity of forest communities across the
oftheAmazonforest andassociatedvegetationtypesto enormousextentofthebasin.Comparedwiththisdiver-
the climatic changes of the last glacial cycle. In the sityofforest,theextentofopenvegetationisverysmall.
process it is necessary to seek evidence of what those ThemassiveplantspeciesdiversityintheAmazonisvery
climatic changes truly were, and we cannot escape the largelyadiversityofforestplants,mostofwhichmustbe
fact that ecological data are also used to establish the expected to have been in existence for far longer than
history of climatic change in the "rst place. The risk of a full glacial cycle. It is the possible reshu%ing of
circular reasoning is obvious. this great diversity over the huge Amazon real estate
Nevertheless, the circle can be broken. A conclusion in response to glacial climate forcing that we seek to
that air temperatures were lower in the tropics can be reconstruct.
disentangled from the pollen evidence for cooling, and It is essential to realize the size and diversity of both
the evidence for CO reduction is quite independent of the forest and the real estate on which it sits. As Fig. 1
(cid:3)
ecological data. The contentious issue of the history of shows, the Amazon drainage, nearly all of it forested,
precipitation in the glacial age Amazon still confounds is spread over an area larger than Europe. At present,
biological evidence for climatic change with ecological only two published pollen diagrams from within the
evidence for plant response to those changes but, even basin o!er a continuous pollen history since early in
with the Was the Amazon ever arid? controversy, we oxygen isotope stage 2, those from Carajas and Lake
` a
should be able to record the main responses to any Pata (Absy et al., 1991; Colinvaux et al., 1996a). When
changes in precipitation that may have occurred, while seekingtodescribetheconditionofthewholebasinfrom
acknowledgingthatquantifyingthosesuspectedprecipi- the evidence of either site it is worth re#ecting on the
tation changes is still not possible. di$culty of using a pollen diagram from Moscow to
The thrust of this paper is to use pollen data to reconstructtheenvironmentalhistoryofParis,anenter-
reconstruct the history of plant communities. It is prise that would involve extrapolating over a compara-
an established principle of modern community ecology ble east}west distance. The possibility for error in
that the unit of response is the species population, not such an extrapolation should be obvious. Nevertheless,
the community or association as a whole (Whittaker, we consider that data so far accumulated are now su$-
1962; Harper, 1977; Davis, 1986; Webb, 1986; Huntley cienttosetasidesomeofthemoreextremespeculations
and Birks, 1983; Prentice et al., 1991; Colinvaux, of the past.
1993a). There are no permanent plant associations,
whether in lowlands or as belts on mountainsides.
Thus ecological theory predicts that the response
among plants to modest changes in climate should be
changes in relative abundance of species within plant
formationstoproduceassociationsmoreorlessdi!erent
fromthosewithwhichwearefamiliarinmodernvegeta-
tion.
Extreme changes in relative abundance can eliminate
a life form, as in the removal of trees from parts of
northernEuropeinoxygenisotopestage2time,allowing
the claim that one formation has been replaced by an-
other (in this case forest by tundra). The most drastic
vegetationchangeinthetropicswouldberemovalof so
many tree populations from a forest that the canopy is
opened, the consequences being caatinga or the savan-
na/grassland known in Brazil as cerrado sensu stricto
(Eiten,1972).Suchfragmentationofacanopyisclassical-
lyattributedtolimitedprecipitation,andhasbeendem-
onstrated to have happened in the Peten of Central
America in glacial times (Deevey et al., 1983; Leyden,
1984).
ClosedforestintheAmazonbasinexistsunderavery
wide span of precipitation regimes, varying from
Fig.1. TheAmazonriversystemandEuropedrawntothesamescale.
'5000mmofrainayearto(1500mmandwithfrom
Extrapolating details of climatic history from one part of so large
a negligible dry season to '5 months without rain aspacetoanotherinviteserror.
P.A.Colinvauxetal./QuaternaryScienceReviews19(2000)141}169 143
2. Modern Amazonian vegetation and pollen spectra pollentaxa.Mostsuchpollenfallstothegroundcloseto
the parent tree, and yet many of these pollen types are
Pollenconcentrationandin#uxintoAmazonianlakes found in lake sediments, presumably carried in the run-
are comparable to, or in excess of, concentrations and o! water of the watershed. The pollen signal of these
in#uxintolakesoftemperatelatitudes(Colinvauxetal., animal-pollinated plants, therefore, records only the
1998), despite early worries that the predominance of community actually growing within the watershed or
zoophilyin tropical forests should result in a depauper- catchment of the local drainage, potentially providing
ate pollen signal (Faegri and van der Pilj, 1979). The a detailed history of a local #ora.
pollen of both the majority zoophilous trees and the Apollensignalforreplacementofclosedcanopyforest
minority of tropical plants that are anemophilous are by open vegetation as postulated by the arid Amazon
wellrepresentedinsedimentsoftheneotropics.Thishas and refugia hypotheses should be clear, as is illustrated
been con"rmed by airborn pollen trapping, particularly bycomparingpollenspectrafromthecerradoofcentral
in the Panamanian forest reserve of Barro Colorado Brazil (Fig. 2) with those from lowland tropical rain
Island (BCI) but also in Amazon lowland forests at forest (Fig. 3).
Cuyabeno,inEcuador,andnearManaus,inBrazil(Bush Fig. 2 is a pollen percentage diagram of glacial and
and Rivera, 1998). postglacial time from a Mauritia palm swamp in the
Widelydispersed,probablymostlyanemophilous,pol- cerradophytopgeographicaldomainintherelativelydry
len types in the neotropics, tend to come from broadly centralBrazilianhighlands,outsidetheAmazonbasinto
de"ned pollen taxa, typically identi"ed only to family the south at Crominia, State of Goias (Ferraz-Vicentini
rank,thathavegeneraorspeciesadaptedtomanydi!er- and Salgado-Labouriau, 1996). The region has a dry
ent habitats. Notable among these widespread taxa are seasonsolongandsevereastopreventtheestablishment
Moraceae,Urticaceae, Ulmaceae,Melastomataceaeand of closed canopy forest except for gallery forests along
Myrtaceaethattogethermakeupasigni"cantpartofthe streams. The present cerrado vegetation is described as
pollenfallingontorainforestlakes.Thetinypollenofthe ..savanna-like vegetation in which the low stratum is
`
moraceous weed tree Cecropia, for instance, can form dominatedby grasses and has scattered shrubs and low
40% of the pollen rain in some Amazonian lakes (Bush twistedtrees,mainlyLeguminosae (Ferraz-Vicentiniand
a
andColinvaux,1988).Cecropiaspeciesarepresentacross Salgado-Labouriau,1996).
thewhole rangeof reasonablymoist vegetationtypes in This cerrado pollen diagram is characterized by 50%
the neotropics, from the lowlands to at least 2000m of grass [Gramineae] pollen in the Holocene samples.
elevation.LikewisethefamilyMelastomataceaehasrep- Surface samples of soil from the gallery forest and from
resentative shrubs and small trees throughout the lacustrine sediments and the swamp surface also had
moisterpartsoftheneotropics,fromthelowlandtropical about 50% grass pollen. The main contributors to the
rain forest to forests high in the Andes. Nevertheless, pollen sum other than grass are herbs of the families
multivariate analysis of pollen percentages of taxa pres- Compositae and Cyperaceae. Input of tree pollen (even
ent as '2% of the pollen sum distinguishes between Cecropia) is little more than a trace, despite the nearby
facies of the neotropical forests (Bush, 1991). presence of gallery forests. A few percent of the ubiqui-
OtheranemophilousAmazontreegeneraincludeIlex, tousMelastomataceaein theabsenceof othertreescan-
Bursera, and shrubs of the family Euphorbiaceae. notrepresentforestandisprobablyaccountedforbylow
More importantly, grasses (Poaceae [Gramineae]), to- melastomeshrubsoflacustrinemargins.TheCyperaceae
gether with other herbs such as Cyperaceae, are pro- record in this core probably emphasizes plants actually
ducersofcopiousquantitiesofwind-blownpolleninthe growingonthebog,asofcoursedoestheMauritiapollen.
Amazonbasinaselsewhere.Podocarpusisanotheranem- HereMauritiagivesalocalhabitat(presenceofaswamp)
ophilous taxon with bladdered pollen typical of many signal.
conifers,butourtrappingdatashowthatpollenoftropi- This cerrado pollen record should be compared with
cal Podocarpus species is not widely dispersed from the thesignalforclosedforestgivenbytheLakePatapollen
parent tree (pollen traps placed almost within sight of percentagediagramin Fig. 3 (discussedin detailbelow).
amontanepopulationofPodocarpusinCerroCampana, In the rain forest pollen spectra, grass and herb pollen
Panama, collected virtually no Podocarpus pollen in is little more than a trace. The bulk of the pollen is
ayear).Thisisquitecontrarytowhatwouldbeexpected dividedbetweenafewanemophiloustreepollentaxaand
of temperate conifers, including high latitude species of a large #ux of diverse zoophilous taxa, most present as
Podocarpus. only one or two grains. A total of 169 pollen taxa were
Taken together, the anemophilous pollen taxa of the identi"ed.Obviouslythepollensignalforclosedforestis
Amazon basin provide a signal for vegetation that ap- utterlydi!erentfromthatofcerradoorsavanna.Ifthere
pears comparable to the classical pollen signals of tem- had been an historical replacement of one plant forma-
peratelatitudes.YettheAmazonforestsyieldinaddition tion by the other, this should be self-evident in a pollen
afarmoredetailedsignalwithadiverselistofzoophilous diagram.
144 P.A.Colinvauxetal./QuaternaryScienceReviews19(2000)141}169
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146 P.A.Colinvauxetal./QuaternaryScienceReviews19(2000)141}169
A general property of Amazonian pollen taxa is that 3. Tropical cooling, lowered CO , and Amazonian plant
2
they cannot safely be assigned to vegetation types. response
Broadly de"ned taxa such as Melastomataceae,
Moraceae, Ulmaceae, Gramineae, Cyperaceae, Ur- Wehavereviewedelsewherethepollenandotherevid-
ticaceae etc. include species that occur in virtually any ence for signi"cant cooling of the neotropics at low
habitat. This redounds particularly on identifying dry elevations during oxygen isotope stages 3 and 2 (Colin-
vegetationtypes.Dryfaciesofneotropicalvegetationall vaux et al., 1996b). The pollen evidence is for large
have thick ground covers of grass and all yield pollen changes in the altitudinal range of plant populations
spectrain whichGramineaepollenispredominant,pos- thought to be sensitive to temperature in Ecuador and
siblyat50%ormore.ThusanyAmazonpollenspectrum Panama, together with the northward advance of
without large Gramineae percentages cannot represent Araucaria forests in southeastern Brazil (Liu and Colin-
dryhabitatsorclimates.Theconverseproposition,how- vaux, 1985; Bush et al., 1990,1992; Piperno et al., 1990;
ever, that high Gramineae always means drying, is Bush and Colinvaux, 1990; Ledru, 1993; De Oliveira,
unfortunatelynottrue.Grassesform#oatingmatsinthe 1992). These data, together with other pollen data from
Amazonsystem,andothergrassesareseasonalcolonists Africa and tropical Asia, provided increasingly persua-
onvarzeasormud-bankislands.Emergentaquaticgrass- siveevidenceforsigni"cant coolingin glacial times.But
esgrowasdensestandsinmanyshallowlakes,andother paleoecologistswerefreedfromhavingtousethepollen
grasses colonize the surface of drying bogs. data to infer temperature depression when independent
Thus grasses, although always associated with open measuresofsea surfacetemperature(SST)inthetropics
vegetation, are not index fossils for savannas and cer- and noble gas concentration measures in fossil ground-
rado. Similar interpretationaldi$cultiesplague reliance waterofeasternBrazilboth suggestedcooling(Guilder-
on herbs such as Borreria and Compositae. These taxa sonetal.,1994;Stuteetal.,1995).Sincethenthelowering
contain many weed species, particularly prominent on ofsurfacetemperaturesinthetropicsinglacialtimeshas
bog surfaces and lake margins. Even the genus Cuphea, beenshownbyclimatemodelstobeplausiblelettingitbe
knowntobepresentinsavannasandbeautifullydistinc- reasonable to accept glacial cooling of low latitudes as
tive to pollen analysts, provides common understory a working hypothesis (Webb et al., 1997; Ganopolski
shrubsin moist forests, has species that colonizestream et al., 1998; Gasse and Van Campo, 1998; Stute and
banks or drying bogs and even has species that are Talma,1998;Bushetal.,1999;Stilletal.,1999).Thisfrees
rooted aquatics (data from collections at the Chicago the pollen data of the neotropics from its role as ther-
Field Museum and the NY Botanic Gardens). Despite mometer,andwecanaddressthepollendatato identify
claims to the contrary (Van der Hammen and Absy, theresponseofAmazonianplantpopulationstocooling
1994), Cuphea pollen cannot be used as an indicator of in the order of 63C in glacial times.
savanna.AspotentialindexfossilsofAmazonianclimate Both the Ecuadorian and Panamanian records are
change, Cuphea, Borreria, and Compositae, the most from lacustrine deposits of glacial age at mid-elevations
commonly identi"ed neotropical herbs, are useless. in tropical forests. The Ecuadorian sections are 160km
Two woody plant genera, Curatella and Stryphnoden- apartatMeraandSanJuanBosco(SJB)intheAmazon
dron appear to have only obligate savanna species and lowland forest near its upper reaches between 900 and
could be indicators of savanna, when considered in the 1100m (Liu and Colinvaux, 1985; Bush et al., 1990;
context of the rest of the pollen spectra in which they Colinvaux et al., 1997). Radiocarbon dates on wood
appear. A third genus, Caryocar, has to be used with samples of between 26,000 and 33,000yr BP assign the
more caution, despite being prominent in savannas, be- deposits to oxygen isotope stage 3 (Imbrie et al., 1984).
causethegenusalsoprovidessomeofthelargesttreesin Within this interval pollen, phytolith, and macrofossil
lowland tropical rain forest. datatogetherdemonstratethatsigni"cantpopulationsof
Subjective grouping of pollen taxa by habitat or plantsnowrestrictedtoabove2000}3000mweregrow-
communityaspracticedinthepollenanalysisoftemper- ingatabout1000m abovepresentsealevel(say1100m
ate latitudes is, therefore, unwise and likely to lead above the eustatic low sealevel of glacial times. Among
to error. Is Melastomataceae pollen to be allocated theseplanttaxawerePodocarpus,DrimysandAlnusnone
to lake margin shrubs so small that they are part of of which occur on the lower slopes of the Andes today.
the forb layer, to high elevation bushes, to understory A clear distinction needs to be drawn between the
treesofthewettestrain forest?Whenseekingto identify general altitudinal descent of species and the movement
plant formations (is it savanna, forest or shrubland?) of whole plant communities sensu Van der Hammen
Amazonpollentaxamustbejudgedbythecompanythey (1974).In the former,speciesrespondindividualistically,
keep. Extended discussions of the interpretation of accordingto their physiological constraints,invade new
Amazonian and neotropical pollen diagrams can be areas, and die out or are reduced in portions of their
found in Colinvaux et al. (1999) and Bush and Rivera formerrange. Because notwo species haveprecisely the
(1998). same ecological tolerances, climatic change induces
P.A.Colinvauxetal./QuaternaryScienceReviews19(2000)141}169 147
constantly changing assortments of species. Thus the cal forest, which accordingly maintained viable popula-
MeraandSJBpollenspectradonotimplythedescentof tions.Butaminorityoftaxacameunderthermalstressin
whole plant communities,as required by the hypothesis thelowlandswhileexpandingtheirpopulationsathigher
of descending belts of vegetation down mountainsides elevations to yield the modern patterns of distribution
proposedbyVanderHammen(1974).AtMeraandSJB and abundance.
many taxa of the lowland tropical forest remained (see Evidence for reassortment of plant communities with
particularly Bush et al. (1990) for a discussion of forest postglacial warming is also present in the scant pollen
taxa and for an analysis of why these assemblagies of records so far available from the Amazon lowlands. At
pollen,phytoliths,and macrofossilscannotbe the result LakePata(Figs.3and4)pollendatashowthatasigni"-
ofpost-depositionalmixingof#oras from di!erentelev- cant population of Podocarpus was present in isotope
ations).Whatisimpliedischangedforestcommunitiesso stage 2 but disappeared in the early post glacial (Colin-
thatPodocarpusandDrimysgrewinthelowlandforestof vauxetal.,1996a).OnespeciesofPodocarpus(P.lamber-
those times, while Alnus grew on the banks of the forest tii) is currently found in the lowlands of Amazonia,
stream. A parallel descent of temperature sensitive taxa though at low population densities. Nevertheless, the
is shown even more unequivocally in the Panamanian PodocarpusintheLakePatapollenrecordcancon"dent-
records at La Yeguada and El Valle. ly be attributed to species at present restricted to high
The sediments at Lake La Yeguada (700m) yield elevationsbecausethreepollentypes,apparentlyrepres-
a continuous pollen record from '14,000BP, thus enting di!erent species of Podocarpus compatible with
spanningfromisotopestage2untilthepresent(Piperno thearrayofspeciesknownfromhighonPicadaNeblina,
et al., 1990; Bush et al., 1992). The 55m long core from butnotwiththemodernspecieswhoserangeextendsto
the El Valle basin (500m) extends from well before the lowlands, were identi"ed in the Pata sediments.
radiocarbonin"nityuntilshortlyafter8000BP,whenthe With the disappearance of Podocarpus pollen at Pata
lakedrained,thusspanningatleastisotopestages3and camechangesinotherpollenpercentagesalsosuggestive
2 as well as the early Holocene (Bush and Colinvaux, of loss of population by other heat intolerant taxa. Re-
1990).BothsitesareonthePaci"c(southern)sideofthe duction of Podocarpus in the lowland Amazon forest in
cordillera as it passes through Panama, both sites are theearlyHoloceneisalsosuggestedbyapollendiagram
forestedtoday,thoughLaYeguadaisdrierbecausepart- spanningthe late glacialto early Holocenetransition at
lyinrainshadowfromthePaci"c.AsattheEcuadorian Lake Curuca, NE of Belem near the mouth of the
sites,pollenandphytolithdatashowpopulationdescents Amazon River (Behling, 1996 Fig. 4). At Carajas (Figs.
ofsometaxaintheorderof1000minglacialtimes.Both 4and7),thelongpollenrecordisnotableforremarkably
pollen records demonstrate extensive populations of largepercentagesofIlexinglacialtimebutnearabsence
QuercusgrowingaslowastherimoftheElVallecaldera intheHolocene(Absyetal.,1991).Ilexisoneofthetaxa
(600m).Phytolithsdemonstratelowaltitudepopulations withdrawnfromtheLakePatarecordintheearlyHolo-
of Magnolia and of what are now alpine grasses. Other cene,alongwithPodocarpus.Thusthefewpollendatawe
taxa more typical of cooler or montane environments have from glacial times in the Amazon suggest that
included Ilex, Thalictrum, Symplocus, Ranunculus, Val- anumberofheat-intolerantspecieswerenoticeablydim-
eriana,RumexandGunnera.AsinEcuadorianAmazonia, inished, or actually removed, from lowland forest com-
however, the pollen data also demonstrate continuing munities by Holocene warming.
presence of tropical forest taxa, including Luehea, Mor-
toniodendron,Bocconia,Erythrina,Dipteryx,Bursera,War- 3.1. The ewects of changing carbon dioxide concentration
szewiczia, Trichanthera gigantea and Bombacopsis
quinata. This was a reassortment of plant communities, CO concentrationintheglobalatmosphereisknown
(cid:3)
not a descent of vegetation belts. tohave#uctuatedinsynchronywithglacialcycles,being
These results are best understood by considering the lowerin the prolongedglacial intervalsthan in thebrief
orderinwhichthereassortmentsactuallytookplace.The interglacials (Leuenberger et al., 1992). With postglacial
beginningwastherelativelycoolglacialtimesofoxygen warming CO concentration rose from 0.02% to the
(cid:3)
isotope stages 3 and 2, when lowland forests of coastal preindustrial Holocene level of 0.03%. Because CO is
(cid:3)
PanamaandthewesternAmazonbasinwerethehabitat the raw material of plant production, and because in
of both the plants of the modern tropical forests and of brightlightCO concentrationsetsthelimitstoproduc-
(cid:3)
extensivepopulationsof a fewplants thatwenow think tivity, when water, nutrients, or temperature do not, it
of as montane. The decisive environmental event was seems inescapable that the rise in CO in the early
(cid:3)
warmingattheonsetoftheHolocene,whentemperature Holocene should have altered, if only subtly, previous
was raised in the order of 63C, a condition not experi- patterns of distribution and abundance.
enced since the time of isotope substage 5e nearly an ThemostobviouspossibilityisthatplantswithC4,or
hundredthousandyearsearlier.Thiswarmthwaswithin crassulacean acid metabolism (CAM), should have had
thetolerancesofmostoftheplantsofthelowlandtropi- acompetitiveadvantageatglacialtimesoflowCO over
(cid:3)
148 P.A.Colinvauxetal./QuaternaryScienceReviews19(2000)141}169
Fig.4. SketchmapshowingprincipalAmazoniansitesmentionedintext.Me"Mera,Sj"SanJuanBosco,Ka"Katira(Rondonia),Pa"Lake
Pata,Ca"Carajas,Fa"Amazonfan.
C3 plants because the reaction constant of the enzyme con"nedtohabitsorhabitatsofunusualwaterstress;to
PEPCarboxylaseusedforcarbonuptakebytheseplants life as epiphytes or on thin soils on rocks (Winter and
appears to extract CO against a steeper concentration Smith,1996).SavannagrassestendtobeC4(becausealso
(cid:3)
gradientthandoestherubiscoenzymeusedbyC3plants. adaptedtodryhabitats),butifgrasslandsreplacedforest
A prime objection to this argument, however, is that theevidenceshouldbeclearinthepollenrecord,whichis
mostoftheworldsplants,andessentiallyalltrees,areC3. examined below.
TheseC3plants,includingthevastmajorityoftheplants The expectation that C4 and CAM should have had
of the Amazonbasin, apparentlydid well enough in the a compelling competitive advantage in glacial times of
Amazon, as over the rest of the earth, in the last pro- low CO has echoes of an earlier debate when, shortly
(cid:3)
longed ice age because they are still with us, still the after the discovery of the C4 pathway in sugar cane by
dominant life forms. Then, as now, the C4 and CAM Hatch and Slack (1979), C4 plants were dubbed
plants } bromeliads, cactus and opportunistically CAM e$cient plants (as opposed to the ine$cient C3
` a ` a
plants like Clusia * would have had their advantage plants), generating expectations of evolutionary change
P.A.Colinvauxetal./QuaternaryScienceReviews19(2000)141}169 149
fromC3toC4tobeinprogressthatwere,however,soon formed by the slow solution of silicates from the parent
refuted (Burris and Black, 1976). The manner of carbon plutonicrocks.Thelakeliesatabout300melevationon
uptake is but one of the many properties that adapt a low inselberg rising above an immense stretch of low-
a plant species to its microhabitat, or its niche, so that landplains,atroughly100melevationandcoveredwith
a change in CO concentration should have a limited lowland tropical rain forest. From a vantage point near
(cid:3)
impact on relative success. Whether signi"cant changes LakePataonecan lookoutoverunbrokenforestasfar
inrelativeabundanceinthehugelydiverseAmazon#ora astheeyecansee.Theinselbergitselfisalsocoveredwith
followed the carbon enrichment of the early Holocene tropicalforest,thoughsomewhatstuntedandmodi"edin
woulddependontheplasticityofphysiologicalresponses places because of shallow soils on the hard rocks that
ofthemembersofthisdiversearray,responseswhichare haveresistedweathering,formingaforestthatisedaphi-
still essentially unknown. cally constrained. A Livingstone piston core shows the
Recentresearchhas concentratedone!ectof reduced sedimentstobenearly7mthick,thetop1.7mspanning
CO athighaltitudeswhenthelowpartialpressureofall thelast40,000radiocarbonyears.Pollenanalysisofthis
(cid:3)
gassesmight be presumedto make the problemsof car- top section provides the "rst history from within the
bon uptake most serious. All trees are C3: might not, lowland Amazon forest through the last glacial cycle
therefore, the C3 treeline be depressed from shortage of (Colinvaux et al., 1996a).
carbon alone (Street-Perrott et al., 1997). Modern tree- TheupperpollenspectraofFig.3areofHoloceneage
lines constitute the formation boundary for which we andillustratethe pollensignalfor lowlandAmazonfor-
havethemostsatisfactorymechanisticexplanation,that est of the kind now present in the area. Four things are
theyaresetbytemperatureactingthroughheatbudgets apparent about this part of the diagram:
of erect plants, or through susceptibility to freezing of
1. The prominence of wind dispersed taxa, for instance
young shoots, or both (Gates, 1968; Tranquilini, 1979).
Moraceae, Urticaceae and Euphorbiaceae (Alchor-
Thesuggestionthattreelinesinglacialtimesshouldhave
nea).
been set by CO concentration rather than, as now, by
(cid:3) 2. Thepresenceofsigni"cantamountsofanimal-pollin-
temperature, is certainly intriguing, but it violates both
atedtrees,suchasCaryocar(Caryocaraceae),Mauritia
the principles of parsimony and uniformity,particularly
(Arecaceae/Palmae); Copaifera (Caesalpinaceae/Leg-
withtheaccumulationofevidencefromlowerelevations
uminosae) and many others.
that cooling was severe in glacial times.
3. When all the tree pollen, including the low counts of
Noneoftheargumentsofthispaperrestonmovements
grainsfoundasatrace(listedas otherarboreal )are
oftree-lines.Thereassortmentsshownbyourpollendata ` a
addedtogether,thetotaltree(arboreal)pollenisinthe
are all between lowland and montane forests and within
vicinity of 90%.
plant communities dominated then as now with plants
4. The very low count of herb pollen, particularly the
usingC3photosynthesis.Eventhegrassesassociatedwith
almost complete absence of Gramineae.
thereassortedplantcommunitiesatMeraandSJBwere
ofC3genera,asshownwithphytolithdatabyD.Piperno Thesefour pollencharacteristicsof theHolocenerain
(Bushet al., 1990). It remains parsimonious to conclude forestsoftheL.Patawatershedalsode"nepollenspectra
that the reassortments we "nd in our pollen data are ofglacialtimes,astheyarepresentin sedimentsdirectly
responsestotemperature,withthelargestchangesbeing dated to the CLIMAP last glacial maximum (LGM) at
expulsionofheat-intolerantplantsfromthelowlandfor- 18,000BP and on to the limit of radiocarbon at
est at the onset of the Holocene. 40,000BP.Awatershedrecordofpollenfromzoophilous
trees delivered to the lake by surface run-o! is also
present,includingsuchtropicalforestgeneraasTapirira
4. Ice-age vegetation of the Amazon lowlands Copaifera, Caesalpiniaceae, Lecythidaceae, and Tapirira
[Anacardiaceae]. Of these Tapirira is a genus only of
The only direct evidence for the vegetation of the lowlandforesttrees.Copaifera,whichattains10%ofthe
Amazon lowlands in glacial times comes from pollen pollensuminthemid-Holocene,isagenusoflargeforest
analysisofsediments,eitherfromcatchmentbasinsinthe trees in the family Caesalpiniaceae [Leguminosea-
Amazon lowlands themselves or from sediments depos- Caesalpinioideae]. Twenty-"ve species are known from
itedbytheriversystemontheontheo!-shoreAmazon theneotropics,anyoneofwhichmightberepresentedin
fan (Fig. 4). the Lake Pata pollen diagram. Our pollen data suggest
alocalCopaiferapopulationeventinthewatershedlast-
4.1. Forests of the western Amazon: Pata, Mera, and San ing many tree lifetimes and starting about 6000yr ago.
Juan Bosco We have not yet been able to identify the pollen from
most Caesalpiniaceae and Lecythidaceae below family
LakePataoccupiesa closedbasin withoutsigni"cant rank but both families are well-representedamongtrees
inlet or outlet streams, probably a pseudokarst basin of the lowland rain forest, and Caesalpiniaceaeincludes
150 P.A.Colinvauxetal./QuaternaryScienceReviews19(2000)141}169
forestlianas.TogetherwithTapirirathepresenceofthese shallow portion of the basin now occupied by the
familialtaxademonstratesthepresenceof lowlandrain- Mauritiaswamp,but,ofitself,itgivesnoindicationofthe
foresttreesactuallygrowingwithinthesmallLakePata cause of lake level rise.
watershedfromwhencetheirpollencouldbewashedinto ThehistoryofthelocalMauritiapopulationisnotthe
the lake. only evidence for #uctuating water table of Lake Pata
ThetaxonMauritiaisprominentintheHolocenepor- becauseasedimentaryunitspanningtheLGMisconsis-
tion of the section,but not earlier. Mauritia is a palm of tent with low water level or even intermittant drying of
wetormarshyground,aswellasbeingaprincipaltreeof the basin (Fig. 3). Because of the extremely slow sedi-
gallery forests in savanna areas. It appears to be zo- mentationrateofthisintervalithasevenbeensuggested
ophilous but stands of the trees are very common in thatthatthereisa gap inthesedimentcolumnbetween
` a
marshy areas at the edges of lakes so that their pollen about18,000and30,000yrBP,withtheimplicationthat
tendstobepresentinmostAmazonianlacustrinepollen this gap represents a time of drought (Ledru et al.,
` a
diagrams.Thereis an extensivestandof Mauritia beside 1998).However,datingofasampleintheshortlengthof
modernLakePataandthepollendiagramsuggeststhat core spanning this interval has now yielded an age of
thishas beena featureof the Holocene.In glacialtimes, 22,600$90yrBPandadepth}ageplotusingtheentire
however, the Mauritia stand was not present. This is data set shows that sedimentation has been continuous
a purely local record of a patch of wetland within the over this interval, although slowed (Table 1, Fig. 5).
watershed that might or might not record changed cli- Pollenconcentrationrisesoverthisintervalbyafactorof
mate: increased precipitation could create a swamp for up to 4, suggesting that pollen in#ux was roughly con-
Mauritia, but so could impoundment of drainage or ris- stantdespitethereducedaccumulationofothersedimen-
ing of the water table. The apparent coincidence of the tary materials (Fig. 5). With continuous sedimentation
MauritiariseatLakePatawithastratigraphicchangein demonstrated, it is convenient to replot the Lake Pata
the sediments and the onset of postglacial time gives pollendiagramwithageasthey-axisinsteadofdepthin
strengthtothehypothesisthatthisparticularswampwas core(Fig.6).Thispresentationof thedatashowsclearly
associatedwiththeendofthelastglaciationasincreased thattherearenosigni"cantchangesinplantassociations
precipitation raised the water level creating the swamp across unit B other than the intrusion into the forest of
besidethelake.Persistenceoftropicalforestbothbefore thefewtaxathatwenowassociatewithmontaneforest.
andaftertheestablishmentoftheMauritiaswampshows Sediment unit B, spanning as it does for roughly
thatany changein the rainfall regime cannothavebeen 30,000BP to 15,000BP, closely approximates oxygen
major. Thus the record of Mauritia pollen suggests that isotope stage 2 (Imbrie et al., 1984). The percentage
meanlakelevelroseattheendofglacialtimeto#oodthe compositionofpollenoverthisintervalissimilartothat
Table1
RadiocarbondatesfromtheLakePatainselberg(TheHillofsixLakes)
LakeDraga(cid:1)o LakePata LakeVerde
DEPTH(cm) AGE DEPTH(cm) AGE DEPTH(cm) AGE
2.0 1800$60 AMS 4.0 2420$60 AMS 2.0 12,050$50 AMS
3.0 5370$50 AMS 14.0 2810$50 AMS 7.5 2790$50 AMS
18.0 2290$60 AMS 50}55 5800$70 BULK 12.0 12,480$60 AMS
20.0 8050$60 AMS 62.5 14,230$60 AMS 26.0 17,100$70 AMS
33.0 22,630$120 AMS 67.5 15,560$60 AMS 52.5 16,410$70 AMS
37.0 12,020$60 AMS 72}77 17,840$300 BULK 57.0 18,430$100 AMS
49.0 35,200$240 AMS 73.5 18,020$70 AMS 84.5 19,740$70 AMS
55.0 34,300$590 AMS 76.5 17,850$60 AMS 90.0 19,170$120 AMS
57}62 37,540$680 BULK 81.5 22,600$90 AMS 135.0 18,680$130 AMS
108}113 39,780$990 BULK 84.5 30,830$220 AMS 193.0 23,600$450 AMS
183.5 '46,200 AMS 96.5 32,010$630 AMS 393.0 '43,800 AMS
105}110 31,390$540 BULK
106.5 34,650$420 AMS
113.5 37,830$130 AMS
115}120 38,860$920 BULK
155}160 42,010$124 BULK
Radiocarbonagesofapproximately23,000BPhavenowbeenobtainedfromallthreelakesontheinselbergforwhichwehavecores.Thisageisin
themiddleoftheepriodforwhichLedruetal.(1997)suggestedthattherewerenorecordsfromtheAmazon.Inallthreecores,pollenspectrafromthis
intervalisofclosedlowlandtropicalforestaspublishedforLakePata(Colinvauxetal.,1996a).Thee!ectsofrepeateddryingofLakeDraga(cid:1)othrough
leakage,aswitnessbyour"eldparty,isapparentinadisturbedrecordofHolocenedates.