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Palynological differentiation of savanna types inCarajás, Brazil (southeastern Amazonia)Maria Lúcia Absya, Antoine M. Cleefb, Carlos D’Apolitoac & Manoela F.F. da Silvad

a Coordination of Biodiversity, Instituto Nacional de Pesquisas da Amazônia (INPA), Manaus,Brazilb Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam,The Netherlandsc School of Geography, Earth and Environmental Sciences, University of Birmingham,Edgbaston Birmingham B15 2TT, UKd Museu Paraense Emílio Goeldi (MPEG), Belém, BrazilAccepted author version posted online: 11 Mar 2014.Published online: 24 Apr 2014.

To cite this article: Maria Lúcia Absy, Antoine M. Cleef, Carlos D’Apolito & Manoela F.F. da Silva (2014) Palynologicaldifferentiation of savanna types in Carajás, Brazil (southeastern Amazonia), Palynology, 38:1, 78-89, DOI:10.1080/01916122.2013.842189

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Palynological differentiation of savanna types in Caraj�as, Brazil (southeastern Amazonia)

Maria L�ucia Absya*, Antoine M. Cleefb, Carlos D’Apolitoa,c and Manoela F.F. da Silvad

aCoordination of Biodiversity, Instituto Nacional de Pesquisas da Amazonia (INPA), Manaus, Brazil; bInstitute for Biodiversity andEcosystem Dynamics, University of Amsterdam, Amsterdam, The Netherlands; cSchool of Geography, Earth and Environmental

Sciences, University of Birmingham, Edgbaston Birmingham B15 2TT, UK; dMuseu Paraense Em�ılio Goeldi (MPEG),Bel�em, Brazil

Pollen rain studies in Amazonia are scarce but of utmost importance to support interpretations of pollen records. Wehave investigated modern surface pollen spectra and vegetation in an Amazon location, Caraj�as, Brazil, where openand woody types of vegetation, swamps and lakes develop under rock outcrops. Both plant inventories of differentsavanna types along with bryophytic surface samples were analysed with ecological ordination. The results point totaxa that can be used in the differentiation of dry and flooded systems within the savannas studied. Dry savannas,either open or wooded, are indicated by the herbs Cuphea, Asteraceae, Borreria, Caryophyllaceae and Polygonaceae,and by woody taxa such as Myrtaceae, Byrsonima, Sapotaceae, Neea and Rubiaceae. Flooded savannas (swamps)and lakes are indicated by herbs like Sagittaria,Montrichardia, Nymphaea, Cyperaceae andMimosa and palms. Poa-ceae was found to have a bipolar signature, and using it as an indicator should be done with caution.

Keywords: Amazonia; pollen rain; savanna; Caraj�as; Brazil

1. Introduction

Pollen records are usually the only means for analysing

past vegetation conditions, particularly in the Amazo-

nian lowlands where extensive dense forests cover an

immense area and impede rocks with other fossils from

becoming exposed. Hence, much tropical palaeoeco-

logical reconstruction is dependant on drill cores, such

as those from lakes and swamps, and the interpretationof the pollen therein. An example of the importance of

pollen records in the Amazon is the long debate con-

cerning late glacial forest conditions (Hooghiemstra &

Van der Hammen 1998; Haberle & Maslin 1999; Bush

et al. 2004; Anhuf et al. 2006). In many instances,

interpreting such records is debatable partly due to

lack of calibration from modern pollen studies in the

same areas. Accurate interpretations of such recordsare also difficult because they depend on adequate pol-

len identifications, knowledge of processes of pollen

deposition into sediments, as well as relations between

pollen spectra and their parental vegetation. Despite

such difficulties, it has been shown that identification

of ecosystems and habitats using pollen spectra is feasi-

ble (Bush 1991; Gosling et al. 2009; Burn et al. 2010;

Ortu~no et al. 2011) and that it holds increasing poten-tial for more robust reconstructions.

The notion that the two pollen groups – trees and

herbs – are sufficient to interpret palaeoclimates has

long been discarded. This is due to the fact that some

wooded habitats in dry areas can have a majority of

coverage by trees and low herbaceous abundances.

Conversely, herbs such as grasses are not unique toopen and dry ecosystems like savannas; for instance,

they can contribute massively to the pollen spectra in

river banks or “floating meadows” (Absy 1979) and

other marshy areas, so much that their use as a palaeo-

climatic indicator can be misleading, making other

taxa more suitable (Bush 2002). Thus, the dichotomy

between grasslands or savannas and tall forests is a

major complication (Pennington et al. 2000; Goslinget al. 2009). Other herbs may present the same prob-

lem. Indeed, lake surroundings and swamps are usually

rich in herbs, and some of the identifiable taxa in pollen

spectra are shared between these marshy sites and

open, dry ones such as grasslands (e.g., Cyperaceae,

Xyris, Borreria).

Considering all these points together, the need for

accurate methods to separate different types of vegeta-tion using pollen becomes clear if additional robust

interpretations of fossil records are desired. The pres-

ent work aimed to differentiate types of savanna (dry

and flooded) on the basis of pollen spectra in a south-

eastern Amazon location – Caraj�as, Brazil.

2. Area studied

2.1. Physical setting

Serra dos Caraj�as is a range of mountains in the south-

eastern Brazilian Amazon (Figure 1). The elevation of

*Corresponding author. Email: lucia.absy@gmail.com

� 2014 AASP – The Palynological Society

Palynology, 2014

Vol. 38, No. 1, 78–89, http://dx.doi.org/10.1080/01916122.2013.842189

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Serra dos Caraj�as varies from 600 to 800 m on an

undulating plateau, where a series of lakes and bogs is

found. According to differences in depth and trophicconditions, these lakes exhibit open water and different

stages of swamp vegetation, from seasonally to perma-

nently flooded.

The annual precipitation in the Serra dos Caraj�asvaries between 1400 and 2000 mm, with a prominent

dry season between August and December (Figure 2).

The mean annual temperature ranges from approxi-

mately 26 �C in the lowlands (ca. 200 m) to 23 �C atthe summits (ca. 800 m).

2.2. Vegetation

The vegetation of Serra dos Caraj�as has been studied,

amongst others, by Silveira (1908), Cavalcante (1970),

Pires (1973), Secco & Mesquita (1983), Silva & Rosa

(1989), Silva et al. (1986a, 1986b), Porto & Silva (1989),

Morellato & Rosa (1991) and Cleef & Silva (1994).

According to Cleef & Silva (1994), rainforest is the

dominant vegetation of Caraj�as.However, the rainforest is substantially drier (from

25% to more than 100%) than most central and western

Amazon forests. Other vegetation types occur there

such as oligotrophic floras on white sand called cam-

pina and the cerrado with a greater amount of xero-

morphism, thick barks and tortuous branches with

short internodes (Pires & Prance 1985). These floras

are floristically and physiognomically different, andrich in endemic species. In general, denser forests are

found at more dissected areas such as slopes, where

soils are thicker and moisture is available for longer,

and open vegetation on higher elevations where soils

are shallow, rock outcrops are visible and water from

rain drains quickly. The vegetation over rock outcrops –

iron deposits – has been referred to as “canga vegeta-

tion” (Secco & Mesquita 1983; Silva & Rosa 1989) and“campo rupestre” (Joly 1970). Both terms can be used

to designate the same type of open, herbaceous patches

of vegetation, with very few or no trees. Furthermore,

despite being within the Amazon domain, Caraj�asshares many similarities with central Brazilian cerra-

dos. Pires & Prance (1985) noted that extra-Amazo-

nian species, such as Pilocarpus microphyllus, and the

extra-Amazonian genus Callisthene, are common inthe Caraj�as savanna forests. The maintenance of these

Figure 1. A: A map of South America and the location of Caraj�as, Brazil. B: Topography of the Caraj�as mountain range and itssurroundings. C: A sketch map showing the main locations within the Caraj�as reserve and mining areas. Notice that islands ofopen savannas “campo rupestre” are found within dense forests and woody savannas (not depicted).

Figure 2. Mean monthly precipitation and temperature(circles) at Caraj�as, Brazil; data are from 1960 to 2000(Source: http://www.cru.uea.ac.uk/) (Mitchell & Jones 2005).

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savanna physiognomies is due not only to edaphic but

also climatic conditions of marked seasonality

(Figure 2).

Diverse habitats have been named by Cleef & Silva(1994) to differentiate savanna forests and lakes. Some

of these include swamps, otherwise termed hydroseral

vegetation. Every habitat has some peculiarities of

both floristic composition and structure; for instance,

some swamps can be largely dominated by grass and/or

cyperaceous herbs, whereas others show clusters of

palms and ferns. Aquatic plants are also abundant and

diverse in lakes and swamps. For a detailed list andexplanation of plant communities found in Caraj�as, seeCleef & Silva (1994). For the present study, we adopted

the following simplified terminology: (1) open savannas

are the summit and dry slope communities where flood-

ing does not exist or is extremely rare, and comprises

both grasslands and bare rock surfaces with few plants

(campo rupestre); (2) woody savannas are open to

closed savanna forests (cerrado/cerrad~ao); (3) swamps

are the hydroseral communities (savanna lakes) that

are subject to constant or periodic flooding and include

palm swamps; and (4) lakes are open-water communi-

ties, rarely drying out and thus permitting long-term

aquatic populations. Dense ombrophilous forests were

not surveyed here. Some key features and taxa for these

communities (1 to 4) are listed in Table 1.

3. Methods

3.1. Fieldwork

The fieldwork was performed during an expedition in

1988 to the south and north areas of Caraj�as. In total,

45 surface (bryophytic) samples were taken for palyno-

logical analysis at the same sites where 45 plots of the

different types of natural summit vegetation (see Sec-

tion 2.2) were described by Cleef & Silva (1994). These

plots were sampled in the Serra Norte dos Caraj�asclose to the Rio Doce Geologia e Minerac~ao S. A.

(DOCEGEO) camp and in the Serra Sul dos Caraj�asnear lakes 8, 9, 10 and 19 (Figure 1C). The methods of

vegetation sampling followed Cleef (1981) as applied

to the Colombian p�aramos. The distance to the rain-

forest border on the slopes varied up to approximately

1 km. After selection and delimitation of a homoge-

neous vegetation type, 10 to 20 (depending on the plotsize) small samples of bryophytes (occasionally lichens

and the uppermost part of the litter layer) were taken.

The pollen samples were stored in plastic bags, closed

and transported to the University of Amsterdam.

For all species present in each of the 45 plots the

external coverage was estimated. This was done by

estimating separate canopy surfaces and the percent-

age of the area covered by shrubs and by the herba-ceous and ground layers. The size of the plot area

Table 1. Subdivision of the main vegetational domains surveyed comprising a brief description for each domain and its key taxa.

Community �plots of C&S Key features Key taxa

Rainforest – Zonal vegetation coveringlarge areas, drier thanwestern Amazon forests

–

WoodySavanna

864, 870, 918, 857 Moderately closedcanopy, with trees3–15 m high

Callisthene minor, Pouteria ramiflora,Eugenia flavescens, Ourateacastaneifolia,Mimosa acustipula,Cochlospermum orinocense,Myrciaspp., Begonia guianensis, Alchorneasp., Cuphea sp.

Opensavanna

856, 861, 862, 863, 880, 881, 886,892, 905, 915, 917, 919, 923

Open treelet-scrubsavannas; rock surface,thin, shallow to absentsoils; dry slopes; opengrasslands

Byrsonima coriacea, Croton spp.,Poaceae, Borreria spp., Asteraceae,Cuphea spp.,Mimosa spp., Neea sp.,Vellozia glochidea, Erytroxylonnelson-rosae, Dyckia sp., Noranteaguianensis, Abrus sp.

Swamps 853, 854, 855, 858, 860, 865, 866,868, 869, 878, 879, 882, 883, 884,885, 887, 888, 889, 890, 891, 893,894, 895, 897, 898, 900, 901, 902,903, 904, 906, 908, 909, 910, 911,913, 914, 916, 921, 877A, 878A,889A, 891A, 895A, 914A

Savanna lakes andhydroseral vegetation;herbs-dominated, veryfew trees; fern-palmcyperaceous-gramineous swampsalong shores andseasonally flooded areas

Cyperaceae, Echinodorus sp., Poaceae,Sagittaria sp., Eriocaulaceae,Callophyllum sp., Xyris sp.,Ludwigia,Mauritia flexuosa,Mauritiella armata Blechnum sp.,Styrax pallidus, herb dominateMimosa sp., Borreria sp., Utriculariasp., Chamaecristae sp., mavritiellaarmata

Lakes 858, 871, 872, 873, 874, 875, 876,877, 912

Open water up to 3 mdeep

Cabomba sp.,Mayaca sp., Nymphaeasp., Echinodorus sp.

�Reference numbers of plots as in Cleef & Silva (1994).

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varied according to the structure of the vegetation,

between 2 m2 in aquatic vegetation, up to 16 m2 in

hydroseral vegetation, and from 100 m2 in open sav-

annas up to 150 m2 in savanna forests. Each plotbelongs to one of the plant communities studied by

Cleef & Silva (1994) that are represented by one or

more plots ranked according to their structure, com-

position and ecology. Botanical collections were

deposited and identified in the Emilio Goeldi

Museum, Par�a, Brazil.

3.2. Laboratory work

Palynological analyses of the surface samples were car-

ried out by the first author at the University of Amster-

dam, where an extensive Neotropical pollen reference

collection is available.

The preparation of the surface samples for pollen

analysis included: (1) treatment for 10 minutes with

boiling 10% aqueous potassium hydroxide (KOH)solution (Faegri & Iversen 1989); (2) straining the

material through a sieve (215 mm); (3) acetolysis; (4)

separation of organic material from the sediments by

using a bromoform-alcohol mixture with a specific

gravity of 2.0 (Bennett & Willis 2001); (5) addition of

glycerol to the residue; and (6) evaporation of the alco-

hol for approximately 24 hours at 50 �C. After this

process, the residual material was mounted on glyc-erol-jelly slides for optical microscope analysis. For

each sample, 300 or more pollen grains were counted,

consisting of the total number of arboreal pollen plus

the Poaceae, Compositae, Borreria and Cuphea. Thus,

percentages reported here exclude aquatics and ferns

from the land pollen sum.

3.3. Numerical analyses

Ordination analyses have been extensively used in pol-

len studies (Bush et al. 1990; Burn et al. 2010; Jardine

et al. 2012). They have the advantage of simplifying

data with a high number of variables into few gradients

of variation, thus translating complexity into more eas-

ily understandable means of visualising the data using

a multivariate approach (Legendre & Legendre 1998;Borcard et al. 2011). Here, we use the same multivari-

ate technique to explore vegetation and pollen rain

data, i.e. nonmetric multidimensional scaling (nMDS).

Prior to running the ordination, in order to minimise

the effect of overrepresented taxa, data were trans-

formed with a double standardisation technique, which

standardises both rows and columns of the data matrix

(van Tongeren 1995). The main reason for this choicewas to include aquatic taxa, which are not counted

within land pollen, but are important to the goals of

the present study. Thus, transforming the data was

essential to enable us to utilise the entire dataset. In

particular, the double standardisation is remarkably

effective because, in its first step, it sets 1.0 as the maxi-

mum abundance of each taxon and scales the rest ofthe abundance data accordingly. This prevents some

taxa with extremely high pollen counts to become out-

liers. Furthermore, because pollen can be dispersed

over long distances, we excluded singletons from the

pollen rain dataset; these are quite likely to be mean-

ingless, and only add noise to the analysis. The analy-

ses were performed using vegan (Oksanen et al. 2012)

for R (R Core Team 2012).

4. Results

4.1. Vegetation gradients

A good separation of the main savanna types is

evident from the ordination of vegetation data

(Figure 3). Axis 1 of the nMDS represents the physiog-nomic gradient, which ranges from closed canopy

woody savannas, through different swamp forms, end-

ing up in open-water populations (lakes). Lakes are

best represented by aquatic taxa such as Utricularia,

Nymphaea, Nymphoides, Echinodorus and Sagittaria,

which polarise samples to the positive extremity, fol-

lowed by other herbs such as Xyris, Eriocaulaceae,

Cyperaceae, Aeschynomene, Ludwigia and less evi-dently by Poaceae. Trees, conversely, clearly group

together amongst dry savanna locations, either open or

wooded savannas. Additionally, some herbs are also

important indicators of open or wooded savannas,

including Cuphea, Asteraceae, Lippia, Ipomoea and

Borreria, along with the spiny shrub Mimosa. Poaceae,

and also Borreria to be appear dubious indicator taxa

shared between swamps and dry locations. Palmswamps of Mauritiella armata are also evident; these

occur in specific areas only.

4.2. The pollen signature

The pollen spectra from the different sample locations

produce a less clear result in the ordination, and some

important features can be drawn from this (Figure 4).Most of the swamps cannot be distinguished from

lakes; as can be seen in the ordination (see Figure 4B),

many taxa behave similarly (including Sagittaria,Mon-

trichardia, Nymphaea, Cyperaceae, Mimosa, palms and

some other trees) and cluster samples together. Open

and wooded savannas seem to be more represented by

the herbs Cuphea, Asteraceae, Borreria, Caryophylla-

ceae and Polygonaceae, as well as by woody taxa suchas Myrtaceae, Byrsonima, Sapotaceae, Neea and

Rubiaceae. The Poaceae are shown to indicate both

open and wooded types of habitats.

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4.3. Relationship between pollen and vegetation

The analysis of how the most abundant taxa are dis-

tributed over the sampled locations is further support

of the patterns found with the multivariate approach.

Those taxa suggested to be indicators of their parental

vegetation occur more or less abundantly in each habi-

tat type (Figure 5). Some examples of taxa that prefer-

ably appear in dry-open savannas are Byrsonima,Sapotaceae, Cuphea, Asteraceae and Rubiaceae. How-

ever, in swamps, Cecropia, Trema, Arecaceae,

Mauritia, Celtis, Cyperaceae, Syngonanthus, Sagittaria

and Montrichardia are more frequently observed. The

percentages of Poaceae are high in nearly all sites(mean of 24.8 [2–71]%). Amongst rare taxa (not

shown), one grain of Myrsine is present. Ilex is usually

not present; however, in one sample, it attains over

10% in abundance.

For most of the taxa, there is no correlation, or a

correlation with low confidence level, of plant coverage

values and pollen abundance data (Table 2).

Figure 4. Nonmetric multidimensional scaling of pollen data collected at different habitat types in Caraj�as, Brazil. Left: sampleordination. Right: taxon ordination (shown are taxa � 1%).

Figure 3. Nonmetric multidimensional scaling of vegetation data collected at different habitat types in Caraj�as, Brazil. Left:sample ordination. Right: taxon ordination.

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Figure 5. Pollen percentage diagrams of selected taxa from Caraj�as, Brazil. Percentage values are based on the land pollen sum,which excludes aquatics and ferns. The sample numbers on the left side of the diagram are listed in Table 1 and follow Cleef &Silva (1994).

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Exceptions exist for Cuphea, M. armata, Nymphaea

and Sagittaria. For these four taxa, local pollen abun-dance predicts plant coverage values.

4.4. Spores and algae

Spore counts are not included in the multivariate

analyses because they have not been surveyed in the

dataset. Nevertheless, we report some results on

the distribution of spores. The overall summed abun-

dance of spores in each habitat is similar, and a

statistically significant difference was only found between

open savannas and swamps (p ¼ 0.031). Open savannas

and lakes have the lowest spore counts amongst the four

habitats, with means of 5 (0–14) and 6.5 (0–10), respec-tively. Swamps and woody savannas have high counts,

with means of 69 (0–708) and 71 (6–233), respectively.

Blechnum spores have a high abundance rate – up

to 200% in a few swamp samples. Iso€etes was found in

a few swamp locations, in low abundances. Polypodium

and Schizeaceae spores are present but are rare.

Botryococcus algal colonies were found in both swamps

and lakes.

5. Discussion

5.1. Vegetation gradients

The Caraj�as vegetation was extensively surveyed

between the 1970s and the 1990s (Cavalcante 1970;

Pires 1973; Secco &Mesquita 1983; Silva & Rosa 1989;

Silva et al. 1986a, 1986b; Morellato & Rosa 1991; Cleef

& Silva 1994). From these studies, many species lists

were published as well as details concerning their rela-tionship with the environment (Silva et al. 1996; Porto

& Silva 1989). Here, we aimed to synthesise these vege-

tation data in a way that the could be compared with

pollen rain data. An ideal transect of the different vege-

tation types can be drawn from the ordination analysis

(Figure 6). It shows a distinct gradient from closed-

canopy savannas to savanna lakes. The stress value of

0.138 is a good measurement of the nMDS efficiency. Afew samples, however, seemed to be outliers; these

included samples from the open and woody savannas.

These samples may appear to be similar because of

their close floristic similarity. Many taxa are shared

between open and wooded savannas, such as Byrso-

nima, Callisthene and Bignoniaceae, and some of the

Table 2. Summary results of comparisons of plant coverversus pollen abundance for taxa found in both the botanicalinventory and the pollen rain. Data were log-transformed.Bold values represent the best significant correlations.

Taxa r2 Taxa r2

Abrus �0.02081 Ludwigia 0.1052�

Aeschymomene �0.02311 Malpighiaceae 0.1418�

Alchornea �0.01939 Mauritiena 0.4792�

Asteraceae �0.004134 Melastomataceae �0.007384Bauhinia 0.05283 Mimosa �0.01432Bignoniaceae �0.02298 Myrtaceae �0.004416Borreria 0.05019 Neea �0.02008Byrsonima 0.2637� Norantea �0.02276Callisthene 0.1248� Nymphaea 0.5712�

Caryophyllaceae �0.02273 Nymphoides 0.3124�

Clusiaceae 0.01037 Ouratea �0.003498Croton 0.06887� Poaceae 0.2749�

Cuphea 0.5029� Polygala �0.02182Cyperaceae 0.2782� Sagittaria 0.5655�

Didymopanax �0.01454 Sapium �0.02295Dioclea �0.01662 Sapotaceae 0.2714�

Echinodorus 0.1267� Serjania �0.01677Eriocaulaceae �0.01033 Smilax �0.01448Hippocrattea �0.007888 Utricularia �0.02099Ipomoea �0.02322 Vismia 0.2099�

Lippia �0.0011 Xyris �0.02166

�P < 0.05.

Figure 6. Scores of nonmetric multidimensional scaling (nMDS) axis 1 against an ideal section of vegetation types occurring onthe summits of Caraj�as, Brazil, adapted from Cleef & Silva (1994).

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herbs such asCuphea, Borreria and Poaceae. Byrsonima

and Borreria are more abundant in the open savannas

and often occur in association with Mimosa (Cleef &

Silva 1994), which in Caraj�as is mainly M. acutistipulavar. ferrea, amongst other species. According to Cleef

& Silva (1994), M. acutistipula var. ferrea is well

adapted to the edaphic conditions and dry climate of

the Caraj�as plateaus. Thus, it is abundant in the campo

rupestres or cangas in this area. These particular

edaphic conditions are related to high acidity, low lev-

els of phosphorous, organic matter and soil depth,

which are important variables controlling physiog-nomy (Nunes 2009). The influence of soil depth affects

the vegetation stature, and it is clear from the xeromor-

phic physiognomy of the area that water availability is

also crucial, although this has not this been extensively

surveyed (Silva et al. 1996). All these features seem to

have controlled the gradient from rainforest to the

savanna types and, within the savannas, from woody to

open savannas.The swamps and lakes are characteristic in the

Caraj�as area. They are mostly covered by graminoid

and cyperaceous vegetation, with few trees, except in

some marshes where Mauritiella armata is dominant

and sometimes associated with the fern genus Blech-

num (B. serrulatum according to Cleef & Silva 1994).

The vegetation found in these localities is the expected

hydroseral aquatic and floras.

5.2. The pollen signature

Compared with the vegetation ordination, pollen data

ordination is almost half as efficient (see the stress

value in Figure 4A). This is because pollen can be air-

borne and, given the proximity of the sites sampled, it

is no surprise that some taxa will be broadly repre-sented in the area. Nevertheless, the multivariate

approach gave us the opportunity to rapidly and com-

prehensively characterise these pollen samples. With

few exceptions, samples of open savannas cluster

together, whereas swamps and lakes remain undiffer-

entiated but are separated from open savannas. The

separation of the woody savanna samples from the rest

of the samples is unclear.Perhaps the most striking result in the vegetation

data was that for Mimosa, which was nearly absent in

swamps and lakes, and very abundant in open savannas

in the pollen data, Mimosa was well represented in all

sites. We speculate this result was due to the different

Mimosa species that occur in different habitats. Further

information regarding coverage by each species as well

as pollination and pollen production data are necessaryto solve this question. Other herbs (Asteraceae, Borre-

ria, Cuphea and Caryophyllaceae) seem to be better rep-

resentatives of the open savanna habitats, and not so

much of swamps and lakes. Most of the tree taxa

(Alchornea, Melastomataceae, Cecropia, Callisthene,

Clusiaceae, Trema, palms, Rutaceae, Astronium) are

clustered within the swamp samples. This result is unex-pected and is explained by pollen being widespread.

Some other tree taxa, conversely, are more useful for

differentiating their original habitat – in this case, open

and woody savannas – and these taxa include Myrta-

ceae, Byrsonima, Rubiaceae, Sapotaceae and Neea.

Grass pollen is very abundant in most of the sam-

ples, and its abundance ranges from less than 2% to

more than 71% (mean 24.8%). This variation is spreadamongst all habitats. Open savannas have the highest

mean abundance of Poaceae pollen (30%), followed by

swamps (25%), woody savannas (18%) and lakes

(15.4%). These numbers can now be compared with

other relevant pollen rain studies and added to the dis-

cussion of Poaceae in pollen rain spectra. The use of

Poaceae in characterising modern habitats is extremely

important to palaeoecologists, because Poaceae can bean indicator group of openness in dry habitats. In the

central Brazilian cerrados, Salgado-Labouriau (1979)

found that Poaceae pollen can vary from 50 to 90% in

the pollen rain. Berrio et al. (2000), working in the Lla-

nos Orientales of Colombia, argued that the presence

of gallery forest around a lake located in a wide

savanna area prevents a better representation of this

habitat; however, they still found approximately 20%of Poaceae pollen in a record from a lake surrounded

by forest. Bush (2002) cited many sites in Central and

South America where Poaceae pollen did not exceed

2% in lowland tropical forests. This was 2 to 20% in

semi-deciduous forests and was up to 90% within

savanna systems (Bush 2002 and references therein).

Similar results were also found by Gosling et al.

(2009), who recorded less than 20% of Poaceaein woody savannas of the Noel Kempff Mercado

National Park. These authors, when comparing pollen

trap samples with lake sediments, found that Poaceae

are much more abundant in the latter, and the explana-

tion bears on proximity of the lake sites to wetland sav-

annas. Somewhat similar results were observed by

Burn et al. (2010) in the same region and by Whitney

et al. (2011) in the Pantanal, where high Poaceae pollencounts can be found even with a dense forest near the

sampling sites. These wetland savannas, like in the

Pantanal, can be similar to the swamp samples ana-

lysed herein. The field survey from 19 to 28 September

1988 was performed during the dry season (Figure 2).

Few plants were flowering in the dry savanna, but Poa-

ceae were observed with flowers in areas previously

flooded, where water availability would last longer.Thus, samples from swamps or near swamps are likely

to be over-represented with Poaceae. Considering our

results and comparing them with other studies, we

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agree with previous authors that Poaceae pollen is

rather problematic. We cannot reliably assign its pollen

to open savannas in Caraj�as because swamps also dis-

play a high abundance of grass pollen; hence, pollenrecords cannot rely on the Poaceae abundance to infer

dryness and consequent openness (Bush 2002). Not-

withstanding this, it seems unusual that some samples

from woody savannas that are surrounded by open

savannas have so little Poaceae pollen (three samples

had from 6 to 10%, but one sample had 44%); likewise,

an open savanna sample had as little as 4.8%. The con-

flicting results likely indicate that these forest habitatscan be efficient in damping the pollen rain savanna sig-

nature from the surroundings, such as that found by

Berrio et al. (2000) in Carimagua, Colombia. Finally,

open savannas do not need an exceedingly high abun-

dance of Poaceae pollen to be characterised as such, as

was reported by Salgado-Labouriau (1979) in central

Brazil. Further studies could aim to investigate how

strongly the plateau savannas are represented in pollenspectra within the rainforests in the slopes of the Serra

dos Caraj�as, which is the main ecosystem in the region.

5.2.1. A note on two key taxa

Ilex had not been recorded in Caraj�as, neither in our

field collections nor from herbarium vouchers from the

Emilio Goeldi Museum (MPEG), in Par�a state. How-ever, in a recently performed environmental impact

inventory, an unidentified species of Ilex was found in

a secondary dense ombrophilous forest (AMPLO

2011). Such forests exist near our sampling sites, and

thus the interpretation could be that wind dispersion

brought Ilex pollen grains to the savanna summits.

One single Myrsine grain was found. Botanical col-

lections of Myrsine have not yet been documented inthe Caraj�as summit. We have checked herbarium

vouchers of MPEG and confirmed that M. guianensis

occurs on dry rocky grounds of the Caraj�as hills, whichis particularly important because Myrsine is usually

regarded as an extra-Amazonian taxon from either

central Brazil cerrados or the Andes (Van der Hammen

& Hooghiemstra 2000; Ledru et al. 2001).

5.2.2. Palynological characterisation of the Caraj�asdry habitats

The Caraj�as plateaus are covered by savanna types

that are comparable to those of central and northern

Brazil. They are different from the surrounding

rainforest, and well adapted to both climate and

edaphic conditions. Here, we provide information thatcan be used by palynologists trying to reconstruct

palaeoenvironments, such as that of Caraj�as itself

(Absy et al. 1991; Hermanowski et al. 2012), by

reporting which taxa already identified from earlier

botanical collections are represented in a pollen rain

spectrum and relating them to their parental vegeta-

tion. Like other savannas, the suite of herbs and somespecific tree taxa is diagnostic of this habitat type with

Asteraceae, Cuphea, Borreria and Caryophyllaceae

amongst the herbs, the shrub Mimosa and Callisthene,

Byrsonima and Neea amongst the trees. Most of the

other taxa are commonly found in other pollen records

in the Amazon basin and thus are not suitable for paly-

nological differentiation. Likewise, some of the infor-

mative taxa in the vegetation data are not found or arenearly absent in the pollen data, such as Norantea and

Aeschymomene. However, some well-known cerrado

trees such as Callisthene andNeea, as well as the associ-

ation of herbs (mainly Cuphea and Borreria) with

Byrsonima, provides some confidence that the savanna

pollen spectra presented here is indeed meaningful.

It is also true that the rainforest trees may be contrib-

uting to the pollen spectra. As found by Gosling et al.(2009), dense evergreen forests tend to produce more

pollen than drier habitats like wooded cerrados. This is a

potential bias not covered by our sampling and should

be considered when interpreting and comparing the pres-

ent data. Likewise, moss polsters cover a short period of

time collecting and conserving pollen rain; thus, they do

not display inter-annual differences in pollen production

detectable when pollen traps are used (Gosling et al.2009). Moss polsters, however, may more accurately rep-

resent the vegetation where they occur than do surface

sediments (Wilmshurt &McGlone 2005).

Within the Caraj�as plateaus, several habitats havebeen described, and we investigated whether pollen-

based differentiation is possible. This differentiation is

key to better interpretation of the palaeorecord in the

same site and adds to the ongoing research of palynol-ogy in the Amazon basin.

Lakes and swamps as expected have many simi-

larities that make them group together in the multivar-

iate analyses. Indeed, the dynamic processes of

flooding during rainy seasons in Caraj�as create tempo-

rary lakes and swamps that may connect to each

other. Thus, it is no surprise that differentiating

between these two systems is nearly impossible. Ingeneral, we note that a high abundance of aquatic

plants (including Cyperaceae) with palms is a good

predictor of humid soil conditions. Distinguishing

between wooded and open savannas was not possible;

these two habitats behave in the same manner in the

pollen spectra. The important outcome revealed here

is that, unequivocally, dry (open or woody) and

flooded (swamps and lakes) systems have differencesperceptible in the pollen rain data. This is of utmost

importance for palaeoecologists because it aids the

biased interpretations driven by Poaceae pollen

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percentages when differentiating between regional

openness and local marsh conditions (Bush 2002). We

demonstrate that herbaceous taxa, namely Asteraceae,

Borreria, Cuphea and Caryophyllaceae, in associationwith Neea, Myrtaceae, Byrsonima, Sapotaceae and

Rubiaceae, are good indicators of dry savannas in

Caraj�as. Some of these taxa (Cuphea, Byrsonima and

Sapotaceae) are further supported by the relationship

of plant coverage with pollen abundance (Table 2).

Moreover, it should be noted that Callisthene is found

in wooded savannas (it can attain up to 80% of cover-

age in wooded savannas); hence, its clustering withinswamp samples is misleading, and it is then better clas-

sified as a wooded savanna indicator. The data from

other trees remain dubious and are in need of further

sampling efforts and taxonomic work. Poaceae, as

noted before (see discussion in Section 5.2), is prob-

lematic, but may indicate openness only if supported

by the aforementioned taxa.

5.3. A comparison with the Caraj�as palaeorecord(Absy et al. 1991)

The Caraj�as palaeorecord is amongst the few sites in

Amazonia where data are available for the reconstruc-

tion of glacial conditions. The record shows expansion

of open vegetation during four episodes. Two of these

episodes are particularly conspicuous because they arecoincident with sedimentary hiatuses, during which

herbaceous taxa attain a high abundance, e.g., Poa-

ceae, Borreria, Cuphea, Asteraceae and Caryophylla-

ceae (Absy et al. 1991; Van der Hammen & Absy

1994; Absy unpublished data). The claim that these

taxa are openness indicators was criticised by

Colinvaux et al. (1996) and Bush & De Oliveira

(2006). These groups of authors argued that Poaceae,Borreria, Asteraceae and Cuphea do not necessarily

indicate openness but very local marshy conditions. In

other words, they may represent hydroseral vegetation

in a swamp instead of representing open and dry sav-

annas. We refute this argument by showing that pollen

rain data in the same sites from savanna environments

in Caraj�as support the early interpretations of Absy

et al. (1991) and Van der Hammen & Absy (1994)that these herbaceous taxa do represent open and dry

habitats. The exception is Poaceae, which, as discussed

above, can be a problematic indicator, only useful if

supported by other taxa. We nevertheless hypothesise

that high abundance of Poaceae co-occurring with

other of these indicator taxa in sedimentologically-ver-

ified hiatuses that indicate drier events (Sifeddine et al.

2001) may also demonstrate openness of the surround-ing ecosystem.

The Caraj�as palaeorecord has also been used to

demonstrate cooling in Amazonia (Ledru et al. 2001)

because Podocarpus and Myrsine are found during the

Pleniglacial and Lateglacial. For many authors,

migration of these taxa through high altitudes, such as

a descent from montane biomes to lowlands, is usedas proof of temperature depression. Our finding that

Myrsine presently occurs in Caraj�as raises doubts as

to this interpretation. The genus inhabits dry, rocky

soils on the summits of hills, and we speculate its

expansion in glacial times can be due to dryness-

driven shallowing of the soils, which favored plant

associations adapted to this condition. It would agree

with the edaphic constraints found for some Podocar-

pus species that, as proposed by Punyasena et al.

(2011), can explain their expansion into lower altitudes

during glacial times.

6. Conclusions

Comparing modern pollen rain spectra with modern

vegetation composition on the Caraj�as plateau sup-

ports a pollen-based differentiation of savanna habi-

tats. Dry savannas, either open or wooded, areindicated by the herbs Cuphea, Asteraceae, Borreria,

Caryophyllaceae and Polygonaceae, and by woody

taxa such as Myrtaceae, Byrsonima, Sapotaceae, Neea

and Rubiaceae. Flooded savannas (swamps) and lakes

are indicated by herbs like Sagittaria, Montrichardia,

Nymphaea, Cyperaceae and Mimosa, palms and some

other trees. These taxa were reported to have a wide

distribution in Amazonia and savannas (cerrados andcampos rupestres) but locally can be habitat-specific.

Grass pollen proved contradictory as a habitat indica-

tor and its use is suggested with caution. This assess-

ment shows progress in the understanding of modern

pollen deposition, and helps to elucidate the meaning

of pollen associations found in the Caraj�as palaeore-

cord (Absy et al. 1991).

Acknowledgements

The present paper is the result of a multidisciplinary project,“Paleoclimas Intertropicais”, between CNPq (BrazilianCouncil of Scientific Advancement) and IRD (Institut deRecherche pour le D�eveloppement – France). We are thankfulfor the support of the project coordinators Kenitiro Suguio(University of S~ao Paulo) and Bruno Turcq (IRD). CNPq isalso thanked for financial support. C. D’Apolito thanksCAPES for scholarship process number BEX 0376/12–4.Maria de Nazar�e Bastos and Antonio Elielson Sousa daRocha are thanked for providing herbarium information.

Funding

This work was supported by the Brazilian Council of Scien-tific Advancement (CNPq) [Processes 575747/2008–0,477127/2011–8] and CAPES [scholarship process numberBEX 0376/12–4].

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Author biographics

MARIA L �UCIA ABSY is a research palynologist for theNational Institute for Amazon Research, Manaus, Brazil.She received a bachelors degree in Natural History from theCatholic University of Paran�a (1968), a masters in Botanyfrom the University of S~ao Paulo (1972) and her PhD fromthe University of Amsterdam (1979). Maria’s research usespollen to determine the foraging resources of native stinglessAmazon bees. She also analyses pollen in honey to determinethe food sources of honey bees and honey types. Maria alsostudies Quaternary pollen, and has written several articlesand books.

ANTOINE M. CLEEF is an Emeritus Professor at the Uni-versities of Amsterdam and Wageningen, specialising ontropical vegetation ecology. He has over 40 years researchexperience on the p�aramos, montane cloud forests andAmazon savannas in tropical America. Antoine has studiedthe P�aramo vegetation of Colombia since 1971, and has pub-lished over 160 papers.

CARLOS D’APOLITO is a PhD student at the Universityof Birmingham, UK. His research is on the Neogene andQuaternary palynostratigraphy and palaeoecology of theAmazon Basin.

MANOELA FERREIRA DA SILVA is a botanist at theMuseu Paraense Emilio Goeldi in Bel�em State, Brazil. Shehas over 30 years experience of research on Amazonian eco-systems. Manoela is a specialist on the phytogeography andphytosociology of Amazonian savanna vegetation habitats.

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