Quaternary Science Reviews 76 (2013) 140e155

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Quaternary Science Reviews

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The Hill of Six Lakes revisited: new data and re-evaluation of a key Pleistocene Amazon site

Carlos D’Apolito a,b,*, Maria Lúcia Absy a, Edgardo M. Latrubesse c a Instituto Nacional de Pesquisas da Amazônia (INPA), André Araújo av., 2936, Petrópolis, CEP 69067-375 Manaus, Amazonas, Brazil b Smithsonian Tropical Research Institute, Apartado 0843-03092, Ancon, Panama c Department of Geography and the Environment, The University of Texas at Austin, 1 University Station A3100, Austin, TX 78712, USA article info abstract

Article history: The new analyses of a sedimentary record of Lake Pata in the Hill of Six Lakes, in NW Amazon and its Received 22 November 2011 correlation with other Quaternary proxy records in the region provide new insights regarding the Received in revised form vegetation and climate of the lowland forest during the Last Glacial. Despite what has been reported 9 July 2013 previously in the literature, the sedimentary and pollen records are not continuous. The hill remained Accepted 11 July 2013 forested; however, clear signals of structural change are seen in the record, which indicate that the area Available online experienced a significantly drier climate during the Last Glacial Maximum (LGM). The herbs and taxa that are known to be more dominant in seasonally dry forests were all more abundant during the glacial Keywords: Amazonia part of the record, and the cool-adapted elements were mixed with warm lowland elements, which Palaeoecology indicates a temperature depression. A comparison of the palaeoecological data with other regional Ice age geoenvironmental records of the Upper Negro River basin and other areas of the Amazon provides Pollen additional support for a cooler and more seasonal environment during the middle Pleniglacial, which then became drier during the LGM. A “wet” LGM is strongly refuted; therefore, the palaeoclimatic and ecological models that used the previous proxy data from Six Lakes to sustain “wet” conditions and a “continuous forest record” during the LGM to reconstruct the palaeoenvironmental conditions in the Amazon should be reviewed. Ó 2013 Elsevier Ltd. All rights reserved.

1. Introduction expansion of savannah or other types of seasonally dry vegetation. The exception could be the Six Lakes Hill in the northwest corner of Over the past few decades, a large body of literature has focused Brazil, for which an unbroken forest record during the past w50 on explaining the late Quaternary environments in the Amazon thousand years (ka) before present (BP) is indicated according to basin. Despite the fair contribution of palynology to palae- studies by Colinvaux et al. (1996) and Bush et al. (2002, 2004). They oecological reconstructions, the few scattered pollen sites in the concluded that at this site, a) there was a continuous palynological vast continent-scale territory paint a speculative picture, rather record, b) the main forest change was triggered by a 4e5 C than a conclusive one. The compilation and critical analysis of the regional cooling during the middle and upper Pleniglacial, c) the lowland pollen sites have given rise to many ice age vegetation pattern of precipitation did not change significantly, and d) the maps (Van der Hammen and Absy, 1994; Bush, 1994; Hooghiemstra Amazon persisted “wet” and without any kind of fragmentation or and Van Der Hammen, 1998; Haberle and Maslin, 1999; Thomas, replacement by other types of vegetation communities (Colinvaux 2000; Cowling et al., 2001; Anhuf et al., 2006) that in general et al. 1996; Bush et al. 2004). show the same trend of forest retraction following a precipitation Despite the claim that the Six Lakes Hill was a stable forested decrease as seen in present-day rainfall patterns. area throughout the last glaciation (Colinvaux and Oliveira, 2000, In such reconstructions, the great majority of the pollen sites 2001; Colinvaux et al., 2000, 2001; Bush et al., 2004), some au- indicate dry periods, as indicated by both sedimentary records and thors have argued that the sedimentary record of Lake Pata (one of pollen sequences that mostly show forest openings and the the lakes studied on the Hill) follows the same general pattern shown by Amazon lakes during the Lateglacial and early Holocene (Hooghiemstra and Van Der Hammen, 1998; Ledru et al., 1998; Van * Corresponding author. School of Geography, Earth and Environmental Sciences, University of Birmingham, Birmingham B15 2TT, UK. Tel.: þ44 7919673173. der Hammen and Hooghiemstra, 2000; Mayle and Power, 2008). E-mail address: [email protected] (C. D’Apolito). However, little has been discussed and reported in the

0277-3791/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.quascirev.2013.07.013 C. D’Apolito et al. / Quaternary Science Reviews 76 (2013) 140e155 141 palynological literature on the characteristics of the sedimentary RADAMBRASIL (1976), from Projeto Seis Lagos held by CPRM record of the lake, and some recent palaeoecological papers do not (Viegas-Filho and Bonow, 1976), from colleagues who conducted mention either the additional sedimentary records of Lake Pata that botanical collections at the hill (M. T. Araújo, A. C. Webber and were studied by Santos et al. (2001), Barbosa et al. (2004) and Bruce W. Nelson, personal communication), from herbarium sheets Cordeiro et al. (2008, 2011) or a variety of geomorphologic and from Six Lakes collections (INPA Herbarium-Manaus) and from sedimentological information from the surrounding areas Bush et al. (2004), who commented briefly on their field observa- (Latrubesse and Franzinelli, 1998, 2005; Carneiro-Filho et al., 2002). tions of the composition and physiognomy of the vegetation. At the As claimed by Latrubesse (2012), the “interpretations taking into Six Lakes Hills area, the edaphically constrained vegetation is account just a local record and one “proxy” indicator (pollen) have similar to heath forests of white sands (Whitmore, 1984; also produced a significant drawback in the understanding of the known as Campinas and Campinaranas) not only structurally but Quaternary climatic changes of the South American tropics, in also taxonomically. Nevertheless, given the presence of true dense- special in the Amazon basin”. In the face of this dilemma, we aim to forest trees, bare rock/very thin soil areas and open areas with produce data that are relevant to the understanding of the palae- typical secondary forest elements, the overall vegetation present on oecological dynamics in the Six Lakes Hill region over the Last the hill is better called a mixture rather than generalised as one Glacial period by using the palynological and stratigraphic analyses single type. At several points on the hill, there are swamps where of a parallel core from Lake Pata and by the critical analysis and Mauritia, Mauritiella, Euterpe and Ludwigia are recorded. correlation of Six Lakes with already published multi-proxy geo- RADAMBRASIL (1976) includes the Six Lakes Carbonatite in the scientific results related to other areas of the Amazon. dense forest classification and points out the high abundance of the tree macucu-de-paca (Aldinalatifolia Spruce ex Benth.). Further- more, the following other taxa are reported to be abundant: 2. Setting Alchornea, Ouratea, Melastomataceae, Clusiaceae and Arecaceae. The modern pollen spectra, which were obtained from moss The hill, which is located at 0160Nand66410W(Fig. 1), is polsters during one field session (Bush et al., 2004), show a high composed of Cretaceous intrusive carbonatites (Schobbenhaus, abundance of Alchornea/Aparisthmium, in addition to other com- 1984). Six Lakes is classified as a type of lake that develops on mon forest elements, primarily trees and very few herbs. older terrains without a direct relationship to the fluvial system (Latrubesse, 2012). This type of lake primarily develops on hills or tablelands of older Precambrian rocks that suffered intense 3. Methods chemical weathering over millions of years and that are now undergoing the dismantling of the laterite crust by pseudokarst Our study is based on a new analysis and interpretation of a core processes. Six Lakes Hill is an erosional inverted relief produced from Six Lakes and a comparison with previously published by erosion of the older Brazilian shield rocks. The site is located analyses. w300 m a.s.l. on a large planation surface, which is known in The sediment samples analysed in this survey come from one of Brazil as the Rio Branco-Rio Negro Pediplain (Viegas-Filho and three parallel cores that were drilled in October of 1991 during a Bonow, 1976). research project developed between American and Brazilian sci- The area experiences the typical equatorial warm climate entists in the early 1990s under the coordination of P. Colinvaux (Köppen Af). The northwestern region of the Amazon basin does and E. Franzinelli. As mandated by Brazilian environmental laws, not experience a true dry season: there is no month in which one of the parallel cores was stored as duplicate material at the rainfall is less than 100 mm, and the mean annual rainfall is local institution (the Federal University of Amazonas e UFAM, w3000 mm (Sombroek, 2001). The main source of rain is the Manaus). The field procedures for coring are detailed in Colinvaux moisture brought from the tropical Atlantic by the intertropical et al. (1999), and more information on the drilling methods can be convergence zone (ITCZ) and convective rain (RADAMBRASIL, 1976; found in Bush et al. (2004). The samples were taken to the National Van Der Ent and Savenije, 2011). The limited information available Institute for Amazon Research (INPA-Manaus-AM) for pollen regarding the vegetation of the Six Lakes Hill comes from analysis.

Fig. 1. Map showing the locations of the Six Lakes Hill, Brazil, and other sites discussed in the text: Carajás (Absy et al., 1991) and Maicuru (Colinvaux et al., 2001) (see the text for more details). Manaus is a capital city in the Northern Brazil state of Amazonas. Altitudinal scale is presented in metres; data derived from ETOPO1 (Amante and Eakins, 2009). 142 C. D’Apolito et al. / Quaternary Science Reviews 76 (2013) 140e155

During one excursion in the 1990s by a group from INPA, a moss Table 1 polster near Lake Pata was collected at our request (M.L.Absy) and Pollen rain spectrum from a moss polster, Six Lakes Hill, Brazil. has been properly stored since then. This sample is now used for Taxa % Cecropia 0.9 pollen rain analysis. Protium 26.4 Verbenaceae 0.9 Subsamples were taken at w6 cm intervals, resulting in 42 Moraceae/Urticaceae 10.1 Macrolobium 0.9 Alchornea/Aparisthmium 9.7 Cyperaceae 0.9 samples, each with a weight of w2g.Lycopodium clavatum tablets Anthurium type 6.5 Cissus 0.4 (batch n 177745) were added for absolute counting (Stockmarr, Ilex 5.5 Arecaceae 0.4 1971), following standard methodology: 10% KOH, acetolysis and Clusia 5.5 Anacardiaceae 0.4 heavy liquid separation by bromoform (Faegri and Iversen, 1989). Aldina 4.1 cf Apocynaceae 0.4 The residues were mounted in glycerin gelatin. Three hundred Myrtaceae 2.7 Euphorbiaceae 0.4 Sapotaceae/Trichilia 2.7 Caesalpinioideae 0.4 pollen grains were counted per sample; at the same time, we Monocot cf Araceae 2.3 Sapotaceae 1 0.4 counted other palynomorphs (pteridophyte spores, algae and Aphelandra 2.3 Mauritia 0.4 fungal spores and hyphae), stopping when a total of 300 pollen Menispermaceae 1.8 Poaceae 0.4 grains was reached. Pteridophyte spores were separated into Bignoniaceae 1.8 Burseraceae 0.4 Simaba/Flacourtiaceae 1.3 Ferdinandusa 0.4 different morphotypes and identified when possible, but algae and Sagittaria 1.3 Unkown 4.6 fungal remains were not. The percentages of spores, algae and Myrsine 0.9 Selaginella 0.4 fungal remains were based on the pollen sum. The concentration of Rubiaceae 0.9 Monolete psilate 11.5 algae within the sediments was remarkably high; therefore, 300 Total pollen sum of 216 grains. algal cysts per sample were counted, and the total abundance corresponding to 300 pollen grains was estimated from a simple rule of three. remarkable. The most striking difference is the dominance of Pro- The pollen identification process was aided by the pollen tium (26.4%), which is explainable by the presence of these trees illustrations and descriptions published by Absy (1975, 1979), near the moss polster where it was collected, especially because Hooghiemstra (1984), Roubik and Moreno (1991) and Colinvaux moss polsters serve as pollen rain indicators for only part of the et al. (1999). The Amazon pollen manual and atlas (Colinvaux year (as the moss growth period was not controlled, we do not et al., 1999), which contains photomicrographs and morpholog- know the length of time over which they had been accumulating ical descriptions of the pollen and spores obtained from lake sed- pollen grains). Alchornea/Aparisthmium is present but not as iments from the Six Lakes Hill, significantly aided identification. abundant as in the previous analyses. Contrary to Bush et al.’s However, we relied most heavily on the pollen collection of the (2004) statement that the field observations did not support this Palynology Laboratory of INPA. Recent botanical collections at the taxon as a major contributor to the pollen rain, the recent botanical Hill of Six Lakes assembled by a group from INPA added many new collections at the hill confirm that Alchornea is abundant and, species that could be compared with the fossil types. For ecological hence, is a good indicator for inferring present-day vegetation. information on the identified taxa, we also consulted herbaria Bush et al. (2004) found one grain of Myrsine and we found two sheets from INPA, the Emílio Goeldi Museum, the New York grains. These findings confirm that Myrsine may indeed be a cur- Botanical Garden, the Missouri Botanical Garden and the Herbari- rent contributor to the pollen spectra, unless both we and Bush um of Geneva. et al. have misidentified a related unknown taxon, in spite of the The pollen diagrams were prepared using the R package Rioja fact that Myrsine pollen is quite easy to identify. (Juggins, 2012). A Detrended Correspondence Analysis (DCA) was Many Anthurium pollen grains and another pollen type, prob- performed using the VEGAN package (Oksanen et al. 2011) for R. ably Araceae, were found. Their minimal representation in the fossil The DCA included taxa 2% in at least one sample, and in order to spectrum, however, is probably due to preservation because these minimize further noise, the data matrix was square-root grains are very fragile. Moraceae/Urticaceae is relatively abundant transformed. (10%). In the previous study (Bush et al. 2004), Moraceae/Urticaceae The core analysed here (II) is a perfect parallel to the cores (Ia were recorded at 15% in one sample, out of five, but were generally and Ib) that were previously studied (as described in Bush et al., less abundant. Regarding spores, 25 monoletes were counted as 2004). In addition to the available radiocarbon chronologies well as only one Selaginella, making up 12% of the pollen sum. (Bush et al. 2004), we obtained five new AMS radiocarbon dates in the parallel core. We also compared our record to the three addi- 4.2. Core stratigraphy and chronology tional cores drilled independently by Santos et al. (2001), Barbosa et al. (2004) and Cordeiro et al. (2011). All of the dates were cali- Although the total core totalled 7 m in length, we only analysed brated with Calib 6.0.1 (Stuiver and Reimer, 1993) using the the upper part, from the top (0 cm) to 290 cm (the lowest described IntCal09 dataset (Reimer et al., 2009). level). The uppermost 200 cm are composed of carbon-rich fine- Additionally, we selected some of the samples that were studied grained sediments (identified as black gyttja) with a discontinuous for pollen for analysis of organic carbon and stable isotopes of d13C unit between 60 and 83 cm, which contains sand and nodules and d15N. The analyses were performed at the Duke Environmental (regarded as nodular yellowish clay). A transitional layer between Stable Isotope Laboratory (Duke University e USA) with a Carlo 60 and 63 cm, which is greyish in colour and more or less similar to Erba Elemental Analyzer. the nodular clays, separates the upper black gyttja and the yellowish unit. The upper 60 cm reflects black gyttja, similar to the 4. Results gyttja from 83 to 200 cm, but softer. From 200 to 290 cm, the sediment is brown silty clay. The chronologies of the lake are shown 4.1. Pollen rain in Fig. 2. Fifteen radiocarbon dates were used from the cores described by Bush et al. (2002, 2004), 15 from Santos et al. (2001) The sample of moss polster that was analysed for pollen rain and seven more from Cordeiro et al. (2011). Our five new dates yielded 41 taxa of pollen and only two types of pteridophyte spores (Table 2) are plotted along with the previous ones. (Table 1). The pollen spectrum we found is in general similar to that The cores provide a robust chronology (Fig. 2-A) and show that described by Bush et al. (2004). Several differences, however, are the sedimentation rates during the late Holocene (from w6 cal ka C. D’Apolito et al. / Quaternary Science Reviews 76 (2013) 140e155 143

AB

C D

Fig. 2. Deptheage curves for cores drilled at Lake Pata, Six Lakes Hill, Brazil. A) the cores studied by the present paper and Bush et al. (2002, 2004). B) the core published by Cordeiro et al. (2011) and by (C) Santos et al. (2001). D) Lake Pata and the position of the cores, after Cordeiro et al. (2011) and Bush et al. (2002).

BP onwards) and during the middle Pleniglacial (>45e35 cal. ka BP) The data on a core by Santos et al. (2001) show a general similar are similar, ranging approximately 0.01 cm year 1. However, it is trend in sediment accumulation (Fig. 2-C), but an erosional event notable that the late Pleniglacial (LGM) (w28e14 ka) and the Late- during the LGM is evident from the presence of a sandy layer of glacial (w14e10 ka) are characterised by a) very low rates of reworked sediment. Both of the cores analysed by Santos et al. deposition (ca 0.001 and 0.0007 cm year 1, respectively) and b) a (2001) and Cordeiro et al. (2011) have the middle unit spanning temporal hiatus because part of the record was lost due to erosion. from approximately 35 to 15 cal ka BP (Fig. 2-B). This feature was The most conspicuous of the hiatuses occurs between 35 and 27 cal ka BP, where ca 8000 years are encompassed in 2.5 cm of Table 2 sediment. The second occurs between approximately 17 and Radiocarbon dates from a Lake Pata, Six Lakes Hill, Brazil. 8 cal ka BP, in a probable condensed or eroded phase of sedimen- Sample Conventional 13C/12C(&) Calibrated Lab. Number tation, which results in an almost complete lack of Lateglacial depth (cm) ages (14C yr BP) age (cal yr BP) material. Both hiatuses are marked by lithological changes. 39e41 2440 40 30.2 2710e2350 b-271672 Furthermore, it is also evident that the Holocene had two phases of 55e57 7410 50 25.6 8350e8160 b-271678 accumulation: a) one before 6 cal ka BP characterised by higher 81e83 9790 60 27.2 11,270e11,150 b-271679 sedimentation and b) one after 6 cal ka BP with very low sedi- 110e112 36,720 240 33.0 Outside cal. range b-283083 e b mentation. At the base of the Holocene, erosion may have occurred, 135 137 37,530 260 31.3 Outside cal. range -283082 and events such as the Younger Dryas are not detected. All dates are AMS. 144 C. D’Apolito et al. / Quaternary Science Reviews 76 (2013) 140e155 interpreted as a sedimentary gap during which the lake reached its Pouteria, Bignoniaceae, Ilex, Humiria, Podocarpus, Myrsine, Marc- lowest level, resulting in erosion. A third core cited by Barbosa graviaceae, as well as most of the herbs such as Poaceae and pte- et al. (2004) follows the same trend (core LPT-III in Fig. 2-D), ridophyte spores. There is no apparent change in vegetation with the sandy unit occurring between 25 and 15 cal ka BP. The between the two lithologies. total organic carbon (TOC), water content and carbon isotopic data from these three cores were also analysed. In the sandy unit, there 4.3.3. Zone 2 (82e58 cm) (35e11 cal ka BP) is a much lower concentration of carbon, the water content is also This zone corresponds to the end of the middle Pleniglacial, lower, and the d13C isotopic values indicate a contribution of car- the late Pleniglacial and the Lateglacial (including the end of bon from grass vegetation into the lake system. In addition, a high MIS3 and MIS2). The sediments are nodular clays, with the iron concentration in the sediments indicates an intense erosion of presence of sand indicating clastic accumulation. This zone also the lateritic crust (Cordeiro et al., 2011), which corroborates the includes a small distinct upper layer between 58 and 63 cm erosional event during the dry phase recorded in all of the other (sub-zone 2B) that is somewhat greyish. One sample at 62.5 cm cores. in this short interval was dated by Bush et al. (2004) in a parallel The sedimentation rate of the interval between the deepest two core (Ib) at 17.3 cal ka BP. As reported above (4.2), Zone 2 lacks dated samples in the black gyttja unit was used to estimate the part of the record, which is probably due to erosional hiatuses, basal age at 290 cm. The few analysed samples deeper than 290 cm one of which occurs between 35 and 27 cal ka BP and another are not included here because changes in lithology make age esti- between 17 and 11 cal ka BP. In fact, the interpolated date of mation unreliable. 11 ka as the upper boundary of this zone has a high level of Interestingly, rapid and somewhat clastic accumulations uncertainty. (nodular yellow clays) are also found at another lake in the Six Zone 2 has the lowest pollen concentration of the core, Lakes Hill, Lake Verde (Bush et al. 2004), at which nearly half of the averaging approximately 48,000 grains/g and reaching 37,000 core was deposited between 19 and 22 cal ka. A reversal is evi- grains/g at 69e71 cm (sub-zone 2B), at which the pteridophyte denced by three outlier dates during this sequence, and a gap is spores concentration is higher than the pollen concentration. In identified from 27 cal ka BP to at least 50 ? ka BP (beyond radio- this sample, which is dated to approximately 18 cal ka BP, no carbon dating capacity). algae cysts or fungal hyphae were found, and only 6 fungal spores were found; furthermore, 27% of the grains could not be 4.3. Core zoning identified, most of which were degraded, broken and very translucent. Sub-zone 2-B has no Mauritia, in contrast with 2-A, The 42 samples provided 268 different taxa and an average and spores reach their highest abundance of the entire core at richness of 48 palynomorphs (pollen and pteridophyte spores), this point, with a remarkable peak associated with Blechnum/ ranging from 29 to 73 identified taxa per sample. The pollen dia- Asplenium. The first portion of the zone (2-A 35 to 21 cal ka BP) grams are presented in Fig. 3. An average of 82% (61e95%) of pollen has relatively more algae and fungal remains and fewer pteri- from woody taxa dominate the record; this does not include un- dophyte spores; Podocarpus reaches its highest representation known types, which range from 4 to 27.6% of the pollen sum. Non- (5%) at approximately 18 cal ka BP. From sub-zone 2-A to 2-B, woody taxa ranged from 1 to 14%. The sampling resolution varied several taxa decrease in abundance, such as Alchornea, Moraceae/ throughout the core, ranging around 400e500 years per sample in Urticaceae, Ouratea and Combretaceae/Melastomataceae. How- the first 6 ka and from 35 cal ka BP to approximately 53 cal ka BP; ever, some taxa become more abundant, such as Ilex, Hedyosmum, however, between 6 and 35 cal ka BP, the sampling resolution de- Bignoniaceae and Sapotaceae. One single grain of Alnus was creases due to a series of hiatuses and reaches ca 3 ka at some found. An average of 74% of the pollen identified in Pata 2 points. represent arboreal taxa.

4.3.1. DCA of pollen data 4.3.4. Zone 3 (58e0 cm) (11e0 cal ka BP) The fossil pollen data ordination of Lake Pata supports a sepa- The Holocene is characterised by soft black gyttja. The lower ration of Holocene and late Pleistocene samples. This separation is part of the Holocene (sub-zone 3A) had a markedly slower accu- characterised on axes 1 and 2, which have very similar eigenvalues mulation, 0.0012 cm year 1, whereas the upper Holocene sedi- (Fig. 4), where Holocene samples are grouped at one extremity, ments (sub-zone 3B) were deposited at approximately containing the following taxa: Mauritia/Mauritiella, Caryocar, Are- 0.008 cm year 1. These low rates of sedimentation could also caceae, Cecropia, Sagittaria, Alchornea, Moraceae/Urticaceae and indicate an incomplete record or hiatus: dated samples between Ouratea. In the other extremity, we found the Pleistocene samples, approximately 10 and 6 cal ka BP are scarce to non-existent in the with Ericaceae, Bignoniaceae types, Myrsine, Caesalpinoideae, cores, and several outlets are recorded during this interval. During Apiaceae, herbs (Poaceae and Cyperaceae), and Hedyosmum, the early Holocene (sub-zone 3A), the total pollen concentration is among others. lower, w60,000 grains/g, but becomes very high (an average of w1 million grains/g) in the late Holocene, 6 cal ka BP, and reaches a 4.3.2. Zone Pata 1(290e82 cm) (w53,7e35 cal ka BP) peak of more than 4 million grains/g at a depth of 15 cm. In general This zone comprises samples from the onset of MIS 3 until the terms, the Holocene is characterised by a very high abundance of beginning of the full glacial and is characterised by two different palm pollen combined with Sagittaria, Alchornea/Aparisthmium, lithological units: (1) silty clay and (2) black gyttja, which replaces Ouratea and Cecropia. The late Holocene (sub-zone 3B) has the the clay at 200 cm (sub-zone 1B), corresponding to approximately lowest counts of pteridophyte spores of the entire profile. The first 48.2 cal ka BP. Throughout all of zone 1, we see an average con- sample analysed (9e11 cm) has one single grain of Podocarpus, and centration of 194,000 pollen grains/g. The average concentration of the fifth (29e31 cm) has two grains of Hedysomum. algae is 7.6 million cells/g. The sedimentation rates are low along Our results point to two groups of taxa that behave in different zone 1, averaging 0.016 cm year 1 from w53.7 to 48.2 cal ka BP ways, one of which is more abundant in the Holocene samples and (sub-zone 1A) and approximately 0.009 cm year 1 from 48.2 to the other more abundant in the late Pleistocene samples (Fig. 4). 35 cal ka BP (sub-zone 1B). Some important observed taxa of zone 1 The first group contains mainly Arecaceae, Caryocar, Cecropia, are Combretaceae/Melastomateceae, Myrtaceae, Fabaceae, Sagittaria, Alchornea, Moraceae/Urticaceae and Ouratea, and the Lake Pata tropical lowland forest trees cool-adapted trees

types e 1 e types um Zones type ria ia ages (cal yr BP) Lithology Depth (cm) ocar raceae/Urticaceae taceae ysophlyllumry 0 oute apilionoidea einmania 2,520 Alchornea Mo Ouratea Combretaceae/Myr Aldina Cassia CaesalpinioideaeIlex BignoniaceaBignoniaceae otherProtiumP 2 SapotaceaeChr Cecropia otherCa Sapotaceae/MeliaceaeApocynaceaeLaetiaCaseariaAnacardiaceaeEuphorbiaceaeCordiaBurseraceaeByrsonima typesP otherBombacoideaeRubiaceaeHumirClusia typestypesHedyosmPodocarpusW Myrsine 2,910 10 Melastomataceae 20 3−B 30 40 D C. 6,590 ’

50 140 (2013) 76 Reviews Science Quaternary / al. et Apolito 8,250 3−A 60 17,300 2−B 18,740 70 21,260 27,320 2−A 80 35,220 90 36,600 39,750 100 41,690 110 120 43,200 1−B 130 140 150 45,650 160 170 180 190 200 210 220 230

240 e 1−A 250 155 260 270 280 53,700 ? 290

30 20 10 30 20 20 10 10 10 10 10 10 10 10 10 10

% Black gyttja Nodular yellowish clay Brown silty clay

Fig. 3. Percentage pollen diagrams of selected taxa from Lake Pata, Six Lakes Hill, Brazil. The CONISS dendogram has a total sum of squares scale. Fungal remains refers to fungal spores and hyphae, Algae refers to algal cysts. 145 146

herbs lianas palms/aquatics fern spores

Depth (cm) 0 PoaceaeEricaceaeCyperaceaeAsteraceaeBorreriaOtherHerbaceous herbsWoodyMauritia/Mauritiella lianas lianas ArecaceaeSagittaria otherAsplenium/Blechnum Polypodium types Selaginella.typesMonoleLycopodium PsilateOther spores Fungaltypes remains Algae Concentration (pollen/gram) DCA1 DCA2 10 20 30 D C. ’

40 140 (2013) 76 Reviews Science Quaternary / al. et Apolito 50 60 70 80 90 100 110 120 130 140 150 160 170 180 190 200 210 220

230 e 155 240 250 260 270 280 290

10 60 10 10 80 40 10 10 10 10 90 20 0 1.5 1.5 51015 800 6000

% x1000 x1000

Fig. 3. (continued). C. D’Apolito et al. / Quaternary Science Reviews 76 (2013) 140e155 147

Fig. 4. Detrended Correspondence Analysis (DCA) of pollen data. Samples are shown on the left graph, and taxa are shown on the right graph. The eigenvalues are 0.138 (axis 1) and 0.123 (axis 2). second group is composed of the Bignoniaceae types, Caesalpi- 3.0%), but has higher values at 66, 71 and 76 cm (12e18%). Zone 3 noideae, pteridophyte spores, montane elements and herbs. has values that are similar to or higher than those found in zone 1. The d15N and d13C values were also recorded. Values around 15 4.4. Isotopic analyses 1.5& (ranging from 0.8 to 2.3&) for d N are seen throughout most of the core, but in zone 3, they reach an average of 2.1&, 13 TOC and stable isotopes were studied in some of the samples with peaks of up to 2.6&. The values for d C are similar in zones that were also used for palynology. In general, the TOC content is 1 and 3, with an average of 32&, but spikes of more positive high, with values usually higher than 10% (Fig. 5). Considerably values are seen in zone 2, with values of up to 25&. Two lower values of TOC, 4.7e5%, are found at around 240 cm (zone 1A). samples in zone 2, however, have values around 33&, similar to Zone 2 also has low values of TOC at 56, 61, 70 and 82 cm (2.3e values in zones 1 and 3.

% Carbon δ15N( δ13C(

Lithology Zones ages (cal yr BP) Depth (cm) 2,520±80 2,910±60

3−B 6,590±150 8,250±100 3−A 17,300±315 18,740±140 2−B 21,260±840 27,320±500 2−A 35,220±430 36,600±1530 39,750±1000 41,690±430 43,200±1320 1−B

45,650±2300 150 100 50 0 200

1−A

53,700 ? 300 250 0 5 10 15 20 25 30 35 1.0 1.5 2.0 2.5 −34 −32 −30 −28 −26

Fig. 5. Results of the organic carbon and stable isotope analyses for the Pata record. 148 C. D’Apolito et al. / Quaternary Science Reviews 76 (2013) 140e155

5. Discussion the two upper lithological units (the sand unit beginning its sedi- mentation around 21 cal ka BP and the Holocene unit). 5.1. Sedimentological record 5.1.3. Stable isotopes 5.1.1. Original (Ia) and parallel (Ib) core (Bush et al., 2004) and The organic matter and stable isotope analyses reveal instability parallel core II (present study) in the lake system. All of the proxies seem to indicate that from 27 The dated samples of these three parallel cores provide a robust to 17 ka, the lake had a diminished productivity, with less carbon chronology, from which a clear pattern of sedimentation is evident being accumulated and an incursion of heavier d13C that is inter- (Fig. 2-A). Higher depositional rates are seen from w53.7 to preted to be derived from C4 plants (Meyers, 2003). In a general dry 35 cal ka BP and again from w6 cal ka BP onwards (zone 1). Be- sequence (Fig. 5), this C4 carbon input can be interpreted as grass tween these two phases is the nodular yellowish clay unit (2A and vegetation growing locally. During this period, however, some 2B, including the short grey layer between 60 and 63 cm), which samples have d13C values compatible with those of C3 plants, which occurs between the gap in sedimentation from 35 to 27 cal ka BP shows how unstable the lake was during a time when the changing and another very condensed probable gap at some point from 17 to vegetation was a product of a more seasonal climate. 8 cal ka BP. The interval from 20 to 18 cal ka BP, in the nodular clay The biogeochemical record of Lake Pata that was published by unit, appears to have been one of low deposition. Here, we found Cordeiro et al. (2011) is more detailed. They show generally similar the lowest lake stand, evidenced by very low concentrations of results for the compared period, but lack evidence for the Holocene, pollen and a lack of algae; by lower d15N values that can be inter- which in our record is characterised by a high carbon content preted as a diminished contribution of organic matter from algae; derived from C4 plants and an enhanced contribution of algae seen by evidence of erosion and reworking; and by the peak in spores by the higher d15N values. that is interpreted as erosional accumulation, which leads to se- lective preservation of palynomorphs, as seen by the high amount 5.1.4. Interpretation of the lake record of translucent, unidentifiable pollen grains. At this level, the con- The sequence of depositional events has more precisely dated centration of the spores exceeds that of pollen; we interpret this the changes that the lake system underwent during the past overrepresentation of a robust (thick exine) palynomorph (Asple- w53.7 cal ka BP, which allows reinterpretation. From w53.7 to nium/Blechnum) coupled with poor quality of pollen preservation w35 cal ka BP, the lake level was lower but still high enough to (high degradation) and low concentration as strong evidence of accumulate carbon-rich sediment. The assertion that the lake was reworking (Hall, 1981; Wilmshurt and McGlone, 2005a, b). As at a lower stand level during this period is supported by the noted elsewhere by Wilmshurt and McGlone (2005b), spores are absence of the lower organic layer near the lake edge (core LPT-VI of the most resistant palynomorphs in eroded soils. Furthermore, the Barbosa et al., 2004) and by the biogeochemical data of Cordeiro low abundance of grass pollen at this level may be a result of et al. (2011). We suggest that until approximately 21 cal ka BP, degradation of unidentified Poaceae pollen, whose thin exine de- there was no sediment accumulation along the lake edges. From teriorates rapidly (Cushing, 1967; Hall, 1981; Wilmshurt and w35 to 10 cal ka BP, the lake level reached its lowest phase, drying McGlone, 2005a, b). This may explain the disparity between the up during the LGM and very likely during two other phases (rep- Poaceae pollen abundance and the increase in the d13C isotopic resented by the upper and lower boundaries of the sand unit in signal (this study, Fig. 5 and Cordeiro et al., 2011). This gap is likely pollen zone 2). The coarser sedimentation during this phase and the same one found by Bush et al. (2002) in the palaeochemical the missing record in some areas of the lake are interpreted as þ record of K because algae seems to be responsible for incorpo- erosion caused by storm events in more seasonal climates. This þ rating K into the system, and thus, there is no record of this cation palaeoenvironmental scenario continued until the early Holocene. when the lake dries. The middle-late Holocene exhibited humid conditions similar to There is greater uncertainty with older age ranges, such as those those in the present, with an increasing trend in equatorial hyper- around 43 and 45 cal ka BP. This is due to the limits of the dating humid conditions. method and the consequent difficulties of calibration, which makes In zone 1, the inferred climatic configuration suggests a drier extrapolation of sedimentation rates and ages inaccurate. Hence, and cold condition, as indicated by a lowered lake level and the the age of the bottom of the core is purely tentative. All of the ages presence of cool-adapted (montane) taxa. Such conditions became obtained from the carbon dating method for the three cores (Ia, Ib extreme in Zone 2, where the sedimentological characteristics and II) were utilized, with two exceptions: our w11 and 2.5 cal ka coupled with palynological data (algae concentrations) as well as BP dates seem to be outliers. stable isotope values indicate the drying of the lake and the episodic accumulation of heavier d13C from C4 plants like grasses 5.1.2. Cores of Santos et al. (2001), Barbosa et al. (2004) and (Fig. 5). At this time, the temperature is believed to have reached its Cordeiro et al. (2011) lowest levels, which is indicated by the occurrence of montane taxa The sequence of samples dated by Santos et al. (2001) and such as Podocarpus, Hedyosmum and Weinmania. Nevertheless, Barbosa et al. (2004) reveals a trend similar to those in the previous there seems to be a short phase at w22 cal ka BP, during which the cores, and the sand unit was interpreted as an accumulation gap of appearance of Mauritia/Mauritiella pollen indicates a slightly wetter more than 15 cal ka BP (Fig. 2-B and C). Again, we can see that the event, with swampy to poorly drained conditions in an inferred sand unit is situated between two periods of very low or incom- dominant dry sequence. Finally, the Holocene shows two phases, plete sedimentation (w30e21 cal ka BP and w21 to 12 cal ka BP), with a climate that was probably more seasonal and a lake level and in between these periods, the erosional event occurs. The core that was lower than the present-day level during the early-middle of Cordeiro et al. (2011) has a smaller middle layer that is described Holocene, and with hyper humid conditions since approximately as a discordant contact of brown clay, at which a gap is evident from 6 cal ka BP. w35 to 15 cal ka BP. The differences between these cores are due to different drilling 5.2. Palaeovegetation locations in the lake (Fig. 2-D) and/or the irregularity of the bottom topography of the lake. In fact, one core (LPT-VI Fig. 2-D) presented Major biome changes, such as the replacement of forest by by Barbosa et al. (2004) was drilled near the lake edge and has only savannah, are relatively easy to identify in a pollen record. For C. D’Apolito et al. / Quaternary Science Reviews 76 (2013) 140e155 149 several authors, the near consistency of the pollen assemblage Ericaceae, however, can also be found in other types of forest; for throughout Pata’s history has been interpreted as unbroken forest, example, heath forests such as the Campinaranas of the Rio Negro, with the presence of elements that are presently largely confined to which are recorded to be located <100 m above sea level. montane areas. The late Pleistocene record of the Six Lakes has The present-day pollen spectra at the hill shows Ilex, as well as been shown to reflect a non-analogue collection of vegetation Ericaceae, to be relatively well represented. The Ericaceae genus (Behling, 2001; Colinvaux et al., 2001; Ledru et al., 2001), with a Gaylussacia cannot be distinguished from Agarista (Colinvaux et al., cooling in temperature as the factor that governed the reassorting 1999), and thus, it is questionable whether the fossil type indicates of plant associations. This hypothesis has become a strong cold conditions inferred from the taxa confined to montane vege- ecological belief among palynologists, but it is questionable tation or arid conditions inferred from the present-day distribution whether a cooler and wet climate or a cooler and dry climate of shrubby taxa from Cerrados at which both genera are recorded prevailed. This inconsistency is primarily due to the inaccurate (Von Linsingen et al., 2006). Indeed, Gaylussacia amazonica Huber is interpretations of the sedimentary record presented by several a strong indicator species of Campinaranas e a fact that had not authors (Colinvaux et al.,1996; Bush et al. 2004), who presented the been documented before e and its occurrence could indicate can- palynological record as “continuous” and provided questionable opy openness. Another complication in pollen identification is palaeoclimatic and palaeobotanical interpretations of the Last related to Satyria panurensis (Benth. ex Meisn.) Hook.f. ex Nied., Glacial Maximum conditions. which was collected on the hill and has pollen very similar to that of Gaylussacia/Agarista. We conclude from the overall literature, from 5.2.1. Comparison with modern pollen spectra and herbarium sheets and from oral communications with experienced phytogeographical indicators colleagues that the use of these species as strong palaeobotanical 5.2.1.1. Montane forest indicators. Because they can also be found in indicators of montane forest and cool conditions is refuted on the some montane biomes, Ilex, Humiria and Ericaceae have long been basis of the here presented arguments. Indeed, one could even used as montane forest indicators and are grouped with taxa more argue that Ilex, Ericaceae and Humiria indicate openness, given that often regarded as montane (such as Podocarpus, Myrsine, Wein- they are more common in heath forests in this region. mannia and Hedyosmum) in pollen diagrams such as those of When examining the geographical distribution of Podocarpus, Colinvaux et al. (1996) and Bush et al. (2004). Ilex, Humiria and Myrsine, Hedyosmum and Weinmannia (Fig. 6), it is evident that

Podocarpus spp Hedyosmum spp

* *

6000 1.000 km 1.000 km −20 −10 0 10 20 30 5000 4000

−30 3000 Myrsine spp Weinmannia spp 2000 1000 20 30 0 10

* *

1.000 km 1.000 km −20 −10 0 −30

−90 −80 −70 −60 −50 −40 −90 −80 −70 −60 −50 −40

Fig. 6. Partial map of Central and South America with the botanical collection data for Podocarpus spp, Hedyosmum spp, Myrsine spp and Weinmannia spp. Herbarium data come from the Global Biodiversity and Information Facility (GBIF) and Virtual Herbarium of Flora and Fungi (INCT). 150 C. D’Apolito et al. / Quaternary Science Reviews 76 (2013) 140e155 these taxa occur in a wide variety of sites, ranging from the Central (2010), who compared different vegetational formations in south- American mountains and the Andes to the Atlantic coast in Brazil, western Amazonia. Despite regional differences in the vegetation but are nearly absent in the Amazonian lowland. The area nearest and glacial climate conditions, these studies are the most to the Six Lakes Hill where they are all found together is the comprehensive ones to which comparisons can be drawn. Ac- southernmost tip of the Guyana mountain range (Figs. 6 and 7). The cording to Gosling et al. (2009), the strongest differentiation that most parsimonious interpretation seems to be that these taxa can be made is the assignment of Moraceae/Urticaceae (>40%), migrated to the Six Lakes area in the same event that was related to Cecropia (>3%), Hyeronima and Celtis as indicators of moist ever- the temperature depression. We therefore regard Podocarpus, green tropical forests. While Hyeronima and Celtis are rare elements Myrsine, Hedyosmum and Weinmannia as montane taxa, in spite of in our records, Moraceae/Urticaceae and Cecropia are found in both Podocarpus, Myrsine and Hedyosmum being recorded in lowlands the pollen rain samples and sediments. All six of the pollen rain elsewhere as well (see Van der Hammen and Hooghiemstra, 2000). samples (five in Bush et al., 2004, and one here) are very similar An important issue concerning the occurrence of Podocarpus in regarding the abundance of these two taxa: Moraceae/Urticaceae Amazonia lowlands during the late Pleistocene is that, while it is never exceeds 15% (generally less), and Cecropia is rare; we found generally used as a marker for the upper forest line migration (and only two grains (<1%), and Bush et al. (2004) certainly less than 2% temperature) in montane areas (Groot et al. 2011), its distribution is in only one sample. Based on this, and to the extent that compar- very wide in South America (Fig. 6); for instance, some species isons can be drawn (given the nonsystematic nature of both pollen occur in the gallery vegetation within woody savannahs in central rain studies), the two records indicate a moderate lower repre- Brazil, in other savannah-like vegetation bordering the Amazon and sentation of evergreen forest during the middle to Lateglacial, in the Peruvian lowlands (Ledru et al. 2007 and references cited probably due to mesic conditions at the hill rather than complete therein). This complicates the interpretation of the origin of Podo- tall forest cover. carpus populations reaching the Amazon and allows one to explore Some other taxa have been cited as indicators of certain vegeta- different ways to extrapolate local to regional climate re- tion types such as seasonally dry tropical forest (SDTF) or woody constructions, given that this genus can be a component of both savannah’s pollen rain spectra, and among these, we point out the super-humid and dry vegetation. Furthermore, it has been sug- presence and/or higher abundance in zones 1 and 2 of Machaerium gested that the Podocarpus invasion into lower altitudinal sites in type, Paullinia/Roupala, Myrtaceae, Combretaceae/Melastomataceae ice age Amazonia reflects changes in edaphic conditions rather and Pouteria. In addition to these, Pennington et al. (2000) argue that than solely temperature depression (Punyasena et al., 2011). If this Legumes and Bignoniaceae are typically found in SDTF, and assertion is true, Six Lakes becomes a good model for showing the Punyasena et al. (2008) numerically showed that these two families migration of Podocarpus from nearby mountains (Pico da Neblina, are indicative of drier sites within the Neotropics. Both Legumes and Serra do Aracá and Serra da Anta) (Fig. 7) over the very poor soils of Bignoniaceae are significantly more abundant in glacial-age samples the extensive heath forests in the upper Negro river basin. This than in those of the Holocene (Bignoniaceae: p ¼ 0.00026, df ¼ 39.7; could be an alternative hypothesis that integrates both sets of ev- Legumes: p ¼ 3.8e-08, df ¼ 39.8). idence for cooler and drier glacial settings, as opposed to the view The best indicator of non-analogue vegetation during most of that montane taxa necessarily indicate super humid conditions the Last Glacial period, at least at the very local scale, is Aldina. such as those found in cloud forests. The genus is widespread in the Rio Negro basin and is often cited in the RADAMBRASIL (1976) inventories. In Central Ama- 5.2.1.2. Pollen assemblages and vegetation structure. The best way zonia, A. latifolia is very common and dominates in black-water to calibrate palaeopalynological interpretations is to analyse them flooded forests (Parolin et al., 2004). Several specimens of Aldina under the light of present-day pollen spectra. To date, the most were also collected in the Pico da Neblina National Park, near informative and distinctive pollen rain data for the Neotropical the Hill of Six Lakes; these plants have dry, large-seeded scle- lowland region are provided by Gosling et al. (2009) and Burn et al. rocarpic fruits comparable to those of the Guaiana Shield

Fig. 7. Map of northern Brazilian Amazon with the locations of the sites mentioned in the text. C ¼ Six Lakes; B ¼ Pico da Neblina, Serra do Aracá and Serra da Anta (from left to right); ¼ Aeolian palaeo-dunes (Latrubesse and Nelson, 2001; Teeuw and Rhodes, 2004; Carneiro-Filho et al., 2002). The dashed lines along the upper and middle Rio Negro basin reflect the extension of data collected by Latrubesse and Franzinelli (2005) and ; represent sections dated by radiocarbon. The altitudinal scale is presented in metres; data derived from ETOPO1 (Amante and Eakins, 2009). C. D’Apolito et al. / Quaternary Science Reviews 76 (2013) 140e155 151 legumes (Boubli, 2002). Very recent field observations by bota- drier glacial times could have restructured plant communities nists confirm that Aldina is remarkably abundant in Six Lakes. It significantly, we claim that there is room for the interpretation is clear that the prevalence of Aldina is related to its ecological that during zones 1 and 2, the vegetation at a local scale had a successfulness and plasticity, inferred mainly from the fact that structure that resembles more those forests that are currently it tends to be more abundant in habitats where water stress has found in drier settings. It is obvious that using a blend of the an influence on the physiognomy (e.g., flooded forests and heath most abundant taxa for such interpretations can be misleading forests of Hydromorphic Spodosols). We then assume that because they belong to different vegetation types. Therefore, a Aldina was able to resist climatic changes within the hill by good comparison would be to see how the same controversial being phenotypically plastic and that the temperature depres- taxa behave in other pollen sites in Amazonia, where the vege- sion was not high enough to destabilize the Aldina populations, tational change is clearer. The late Pleistocene record of Carajás whereas climatic changes may have affected other taxa more (w60 cal ka BP onwards) shares some of the most abundant taxa drastically. with Pata (Fig. 8). Alchornea/Aparisthmium, Melastomataceae and palms have generally similar trends in abundance. Alchornea and 5.2.2. Building a scenario palms are abundant elements of the late Holocene and are less After the publication of the first pollen diagram from the Hill of represented during the glacial period; the same is true for Celtis, Six Lakes (Colinvaux et al.,1996), Pennington et al. (2000) raised the which is indicative of moister forests (Gosling et al. 2009). Mel- possibility of a broad expansion of SDTF based on the similarities at astomataceae indicates the opposite, being better represented the generic level of the fossil pollen assemblage at Pata with SDTFs. during the glacial periods (Absy et al., 1991 and Absy, unpub- Bush et al. (2004) refuted this hypothesis based on the distinctive lished data). Poaceae pollen representation in the pollen rain studies of the sa- The strongest difference between Carajás and Pata is that forest vannahs and on the lack of large quantities of charcoal. Moreover, a openness is more evident in the Carajás record during the hiatus pattern of no taxon being overrepresented and a general high between 23 and 12 14C years (or w27 to 15 cal ka years) (Absy et al. arboreal diversity would be crucial for viewing the palae- 1991; Sifeddine et al. 2001). This interval corresponds to the ovegetation at the hill as a clear signal of uninterrupted forest cover, nodular unit in the Pata record; thus, almost all of Pata zone 2 which would be interpreted as a long-term lowland forest biome at correlates with Carajás terminal zone C and zone D (Fig. 8). In the regional scale. addition, the d13C values confirm that although Poaceae pollen does However, for all of the reasons discussed above (5.2.1) and not have clear spikes during zone 2 as argued by Bush et al. (2004) adding the idea that drought in the Amazon basin kills trees in a when they refuted Pennington’s SDTF approach, Poaceae carbon selective manner (Phillips et al., 2009, 2010), a process which in did contribute to the organic matter in the studied record (Fig. 5).

Pata Carajás y

rticaceae g o

/U l

o

h

t i

aceae L Lithology Alchornea/AparisthmiumCeltis Moraceae/UrticaceaeCecropiaArecaceaeMelastomataceae 0 Alchornea/AparisthmiumMor CecropiaArecaceae MelastomataceaeZones 0 Zones E−3 5 5 3−B E−2 3−A 10 10 E−1

15 15 2−B

20 20 D hiatus 2−A 25 25

30 30 hiatus C 35 35 interpolated ages (cal yr BP x 1000)

40 40 1−B B

45 45 A−2

30 20 70 30 30 30 20 10 10 50

Fig. 8. Percentage pollen diagrams of selected taxa from the Pata and Carajás pollen records. 152 C. D’Apolito et al. / Quaternary Science Reviews 76 (2013) 140e155

At Maicuru, a hill similar to Six Lakes in eastern Amazonia JanuaryeFebruary, DJF) precipitation is reduced during preces- (Fig. 1)(Colinvaux et al., 2001), at which a clear sedimentary gap of sional cycles, which causes episodes of lake lowstand that would almost 13 ka exists during w28 to 15 14C years BP or w32 to enhance the productivity of planktonic and benthic algae through 19 cal ka BP (Fig. 9), similarities are found for Alchornea/Apar- elimination of or change in the depth of the thermocline. This isthmium, Cecropia, Melastomataceae, and Moraceae/Urticaceae, interpretation of cyclic rise and fall of the lake level is based on a þ following the same trends as mentioned before for the Pata and palaeochemical record that shows the cyclic nature of K peaks and Carajás lakes. algal blooms that coincide with each other at the nodular sedi- It is important to note that the local palaeoenvironmental ments; however, only one peak occurs within the range of C14 dates, interpretation cannot be extrapolated to a broader scale due to the approximately 13e15 cal ka BP, during which sedimentation was extremely mosaic vegetation composition within the region. The very slow and which probably coincided with a sedimentation gap. available information on the forest types of the Six Lakes Hill and This palaeoclimatological reconstruction is hypothetical because surrounding areas, such as that of RADAMBRASIL (1976), shows a the analysis did not consider the temporal hiatus of the LGM and complex scenario of different physiognomies. The two main types relied on a continuous record e which did not existefor correlation are Campinaranas (heath forests) and Dense Tropical Forest; these with the global climatic changes. For instance, our samples at the can be subdivided into other types according to the degree of nodular clay unit presented comparatively low concentrations of canopy openness and topography, such as open and dense forests, algal cysts. Indeed, between 69 and 71 cm core depth, which dates submontane forests and contact zones. to the LGM, no algal cysts were recorded. Hence, during the LGM, The Six Lakes Hill falls within the Forest classification, despite the lake may have dried up for longer periods than brief episodic all its peculiarities, and it is surrounded by the diverse vegetation events. This hypothesis is supported by two peaks of heavy carbon types. Given the regional differences in topography and edaphic incursion into the lake during zone 2-B, representing local grass characteristics that shape plant communities, we argue climate vegetation. It is also possible to interpret Mauritia at w22 cal ka BP change must have affected each eco-region in a particular way. The as indicating a short phase of increased sub-humid conditions upper Negro River basin is well-known for its extensive Campi- (swampy clastic conditions as recorded today in the many lakes of naranas (Prance, 1987) and there is evidence of severe arid con- the Cerrado and Roraima) just before the strong dry lake event; this ditions prior to the LGM and during the LGM and the Lateglacial, may coincide with the period of unstable dune activity during the with sand dune generation within the Negro Basin (Carneiro-Filho LGM reported by Carneiro-Filho et al. (2002). We cannot et al., 2002). Hence, we infer that the most likely regional scenario completely refute the intricate lake-level dynamics, but our data is that of a complex configuration of habitats responding to dry- firmly suggest that eutrophication, and hence algae concentration, ness differently. has a relationship with warm and humid periods. The nearly non-existent present-day dry season is not strong 5.3. Lake level and seasonality enough to cause the lake to dry out; hence, the constant water table allows for high carbon accumulation and good palynomorph Bush et al. (2002) believed that the variation in Lake Pata’s water preservation. This must have been the general pattern since the level was caused by orbital forcing. Wet season (Decembere middle Holocene, as there is no change in the lithology during this period. For breaks in sedimentation to occur, and be reflected in the lithology, one or both of the following would have had to take Pata Carajás Maicuru place: (i) the lake dried out long enough that aerial or sub-aerial *** exposition affected carbon preservation; or (ii) sediment rework- ing, like the one caused by erosion, increased the input of coarser material, such as clastic grains. Both of these scenarios require a remarkable dry season. We disagree with Bush and Silman (2004) who claim that the greatest changes in precipitation during the LGM was most profound in the wet season, with relatively little change, perhaps even wetter conditions, in the dry season which would have little negative impact on the forest. We claim much lower precipitation during the dry season was the main reason for the persistence of lower lake levels, a dry lake and the changes detected in the lake sedimentary record. During part of the LGM the

Age(ka) annual water balance was negative and the lake dried up.

5.4. Geomorphologic and geologic evidence

A variety of information on the Quaternary palae- oenvironmental conditions of the Upper Rio Negro, which is the basin where Six Lakes is located, has shown that the area suffered 45 40 35 30 25 20 15 10 5 0 significant palaeohydrological and palaeoclimatic changes during Erosional event the Last Glacial. Surprisingly, all of the geoscientific information Black Gyttja (clastic sand) concerning the area and surrounding region was neglected by palynologists as they discussed the palaeoecological and palae- Yellowish Gyttja Other inferred gap oclimatic conditions of the Six Lakes record (for example, Colinvaux Clastic sand et al. 1996; Bush et al. 2004), with the exception of Van der with siderite Hammen and Hooghiemstra (2000). The Negro River, one of the mega-rivers of the world in terms of Fig. 9. Lithology and ages of the three sites discussed in the text, Pata (this study plus Bush et al. 2004;*Cordeiro et al. 2011;**Santos et al. 2001), Carajás (Absy et al. 1991) water discharge (Latrubesse et al., 2005; Latrubesse, 2008) and the and Maicuru (Colinvaux et al. 2001). ultimate example of a black water river in the Amazon basin, C. D’Apolito et al. / Quaternary Science Reviews 76 (2013) 140e155 153 suffered drastic palaeohydrological and geomorphological changes rainfall decreased and the fluvial systems had lower discharge than since the middle Pleniglacial (MIS3 and early MIS2) (Latrubesse and ever during the last glaciation (Latrubesse, 2003; Latrubesse et al., Franzinelli, 1998, 2005). 2005), and the dunes in the Rio Negro basin were active in large The late Pleistocene alluvial sediments form a terrace level areas of the Amazon and Roraima states (Latrubesse and Nelson, approximately 14 m in thickness of sandy to gravelly deposits that 2001; Carneiro-Filho et al., 2002; Teeuw and Rhodes, 2004). include plant fragments (stems and leaves), organic matter and Similar hiatuses are also identified at this time from other paly- impregnation of iron oxide (see Fig. 7 for locations). Radiocarbon nological records of the Amazon (Fig. 9). dating of the logs and organic matter provides results that range The record still indicates sub-humid conditions during the from 27 ka to more than 40 ka BP (beyond the radiocarbon range). Lateglacial (14e10 cal ka BP) at Six Lakes and also at the regional This episode of sedimentation was correlated with the middle scale, as indicated by fluvial deposits (Latrubesse and Rancy, 1998; Pleniglacial (Latrubesse and Franzinelli, 1998, 2005). The palae- Latrubesse, 2003; Latrubesse and Franzinelli, 2005) and aeolian ohydrological regime of the basin was tropical, producing super- dune activity in the Rio Negro basin (Carneiro-Filho et al., 2002). mature quartz sands, but the rivers were morphogenetically more Lujanian megafauna and sub-humid conditions persisted in some active, moving sediments coarser than those of today and aggrad- areas of Eastern Amazonia (Rossetti et al., 2004), but in general, ing the fluvial system. This indicates a higher discharge variability Amazonia shows a trend towards wetter conditions and forest re- and more flood energy than occurs in a contrasting seasonal covery that became more pronounced since the middle Holocene. tropical climate. In the upper Rio Negro Basin, the sedimentological The current environmental conditions were only reached after record is similar to the sedimentological-palynological results ob- 6 cal ka BP BP. The modelling of palaeoenvironmental conditions for tained from the watershed between the Caquetá and Negro rivers, the LGM proposed by Cook and Vizy (2006) suggests that season- where drier and more open vegetation covered a larger area than it ality was enhanced in the Amazon basin during the LGM because of does today, but which was probably dominated by some type of a delayed start in the South America monsoon annual period; they forest-like vegetation (Van der Hammen et al., 1992). also suggest that in most parts of the Amazon basin, the total No record of fluvial deposits was found in the Negro basin for annual rainfall was 25e35% lower in the LGM than in the present- the period from w24 to14 ka BP, which indicates an underfit fluvial day simulation. Despite the uncertainties in the model, the general system in a drier climate in the upper basin. A Lateglacial terrace climatic scenario at the basin scale agrees fairly well with the (10e14 ka) composed of abundant clay sediments is recorded, earlier estimations based on proxy data by Van der Hammen and which indicates different palaeoclimatic conditions than those that Hooghiemstra (2000), who postulated a decrease of regional pre- occur today, because the Negro river and its tributaries currently cipitation in the Amazon and around Lake Pata. Indeed, the model transport only an insignificant amount of wash load (clay and silt). provides a reasonable scenario for the climatic conditions sug- In the middle-upper Negro basin, aeolian dunes spread across gested by geoscientific proxy data around the basins that is better thousands of square kilometres (Fig. 7). Dunes are a strong palae- for MIS3 and early MIS2 than for the LGM. For the MIS3 and early oclimatic indicator because they indicate arid conditions as well as MIS2, the results of the climatic modelling by Cook and Vizy (2006) the regional dynamics of the dominant wind patterns. The dunes are in close agreement with the proxy data for Six Lakes (Santos were generated from at least 32 to 9 ka (Carneiro-Filho et al. 2002), et al. 2001), Barbosa et al. (2004), Cordeiro et al. (2011) and those which indicates remarkably drier conditions than at present during of this paper, as well as with the geoscientific information from the last part of the middle Pleniglacial (MIS3), the LGM and the surrounding areas of the Amazon (referenced above) that indicates Lateglacial (MIS2). The dunes also indicate winds blowing from the the reduction of rainfall, a more climatic seasonality, lower river NE towards the core of the Amazon basin. discharges, aeolian activity and changes in the vegetation cover. The climatic model (Cook and Vizy, 2006) fails around Lake Pata 5.5. Climatic conditions during the Last Llacial probably in part due to an overestimation of the orogenic rainfall effects by the Guyana shield and the underestimation of local During the middle Pleniglacial, the Six Lakes record indicates a convective activity (RADAMBRASIL, 1976; Salati and Vose, 1984; tropical climate with more seasonally dry conditions than today. Van Der Ent and Savenije, 2001). However, we consider e in This is in agreement with other records in the basin, such as the agreement with Van der Hammen and Hooghiemstra (2000) e that pollen records in Katira, Carajás, and the lower Caquetá River basin the drier conditions were in general more extreme during the late (Absy and Van Der Hammen, 1976; Absy et al., 1991; Van der Pleniglacial (24e14 ka BP). Hammen et al., 1992; respectively); the fluvial palaeohydrological record in the largest fluvial systems of the Amazon basin 6. Conclusions (Latrubesse, 2003; Latrubesse and Franzinelli, 2005; Latrubesse et al., 2005); the expansion of the sand dunes field in north- The pollen record from Lake Pata has been interpreted as a central Amazonia (Carneiro-Filho et al., 2002); and the presence continuous record of lowland forest in northwestern Amazonia of megafauna in western and east-central Amazonia (Latrubesse during the Last Glacial. The availability of geochronological infor- and Rancy, 1998). Moreover, the Pata lake system may also reflect mation from different cores, however, has made possible a rean- major world climatic events of the Last Glacial period, as shown by alysis of the record, and the integration of geoscientific data with the biogeochemical data from Cordeiro et al. (2008, 2011) and our palynology represents a significant improvement to palae- palynological data presented here. oecological interpretations. The late Pleniglacial (w24e14 cal ka BP) was characterised by We demonstrate that, far from being a continuous record indi- seasonal and dryer conditions, and during part of this period, the cating the permanence of equatorial rainforest in the Amazon ba- lake was completely dry. The strongest signal in the Six Lakes re- sin, as is assumed by several authors, Six Lakes is a remarkable cord is the erosional event that occurred at the LGM. Santos et al. example of a changing, incomplete and complex palaeoecological (2001) and Barbosa et al. (2004) interpreted this event as caused and limnological record through the Last Glacial and the Holocene. by a markedly increased seasonality, with torrential rains and We demonstrate in this article that for almost two decades, Six cooler temperatures, which is typical of more seasonal climates. Lakes was erroneously used as an emblematic locality to illustrate This corresponds very well with our palynological and sedimen- the permanence of the rainforest in the Amazon basin. This inter- tological interpretations of Six Lakes. At the regional scale, the pretation deeply affected conceptual discussions in terms of 154 C. D’Apolito et al. / Quaternary Science Reviews 76 (2013) 140e155 biodiversity models such as the refuge theory and others, which mercury deposition at a remote Amazon location. Nuclear Instruments and e were considered by many to be no longer valuable because of the Methods in Physics Research B 223, 528 534. Behling, H., 2001. Late Quaternary environmental changes in the Lagoa da Curuça assumption that the record at Six Lakes was “continuous” (Bush and region (eastern Amazonia, Brazil) and evidence of Podocarpus in the Amazon Oliveira, 2006). lowland. Vegetation History and Archaeobotany 10, 175e183. Our new pollen analyses and interpretations of the sedimen- Global Biodiversity and Information Facility, 2012. www.gbif.org. Boubli, J.P., 2002. Lowland floristic assessment of Pico da Neblina National Park, tological records, together with the correlation of other regional Brazil. Plant Ecology 160, 149e167. evidence, show that the Six Lakes Hill was a site with altered forest Burn, M.J., Mayle, F.E., Killeen, T.J., 2010. Pollen-based differentiation of Amazonian in a drier region during a substantial part of the Last Glacial; more rainforest communities and implications for lowland palaeoecology in tropical e w e e South America. Palaeogeography, Palaeoclimatology, Palaeoecology 295, 11 18. precisely, during the middle Pleniglacial ( 60 35 ka MIS3) and Bush, M.B., 1994. Amazonian speciation: a necessarily complex model. Journal of the late middle Pleniglacial (late MIS3) and LGM (MIS2). The record Biogeography 21, 5e18. of Six Lakes is discontinuous and episodic during part of the ter- Bush, M.B., Oliveira, P.E., 2006. The rise and fall of the refugial hypothesis of Amazonian speciation: a paleoecological perspective. Biota Neotropica 6, 1. minal MIS3 and the MIS2, including all the LGM. The palynological Bush, M.B., Silman, M.R., 2004. Observations on Late Pleistocene cooling and pre- record indicates that the vegetation lacked some characteristics of cipitation in the lowland Neotropics. Journal of Quaternary Science 19, 677e684. dense evergreen forests and shared others with the seasonal and Bush, M.B., Miller, M.C., De Oliveira, P.E., Colinvaux, P.A., 2002. Orbital forcing cool-adapted biomes of that time. The triggers of environmental signal in sediments of two Amazonian lakes. Journal of Paleolimnology 27, 341e352. changes were an increased seasonality of rainfall and a general Bush, M.B., De Oliveira, P.E., Miller, M.C., Moreno, E., Colinvaux, P.A., 2004. decrease of annual rainfall that reached a minimum during the Amazonian paleoecological histories: one hill, 3 watersheds. Palaeogeography, e LGM. This is in fact also supported by geomorphologic proxy data Palaeoclimatology, Palaeoecology 214, 359 393. Carneiro-Filho, A., Schwartz, D., Tatumi, S.H., Rosique, T., 2002. Amazonian paleo- (aeolian dunes and fluvial deposits) and palynological data from dunes provide evidence for drier climate phases during the late Pleistocenee the surrounding areas. Holocene. Quaternary Research 58, 205e209. In that area the Amazon rainforest has only just recovered, Colinvaux, P.A., De Oliveira, P.E., 2001. Amazon plant diversity and climate through the Cenozoic. Palaeogeography, Palaeoclimatology, Palaeoecology 166, 51e63. acquiring the present-day physiognomy very recently. Although Colinvaux, P.A., De Oliveira, P.E., 2000. Palaeoecology and climate of the Amazon rainforest is recorded through the entire Holocene, all of the basin during the last glacial cycle. Journal of Quaternary Science 15, 347e356. proxies seem to indicate that the present-day vegetation dates back Colinvaux, P.A., De Oliveira, P.E., Moreno, J.E., Miller, M.C., Bush, M.B., 1996. A long pollen record from lowland Amazonia: forest and cooling in glacial times. to the middle-late Holocene, around 6 cal ka BP. Science 274, 85e88. Colinvaux, P.A., De Oliveira, P.E., Moreno, J.E., 1999. Amazon Pollen Manual and Atlas. Harwood Academic Press, New York. Acknowledgements Colinvaux, P.A., De Oliveira, P.E., Bush, M.B., 2000. Amazon and Neotropical plant communities on glacial time scales: the failure of the aridity and refuge hy- potheses. Quaternary Science Reviews 19, 141e169. This work is dedicated to the memories of Thomas Van Der Colinvaux, P.A., Irion, G., Räsänen, M.E., Bush, M.B., Nunes de Mello, J.A.S., 2001. Hammen and Antonio Rossi. We would like to express our sincere A paradigm to be discarded: geological and paleoecological data falsify the thanks to Elena Franzineli, who kindly provided the sediment HAFFER & PRANCE refuge hypothesis of Amazonian speciation. Amazoniana 16, 609e646. samples. We are much indebted to Henry Hooghiemstra, Francis Cook, K.H., Vizy, E.K., 2006. South American climate during the Last Glacial Mayle and journal editor Neil Roberts for their valuable critical Maximum: delayed onset of the South American monsoon. Journal of reviews. We thank also an anonymous reviewer and Blanca de Leon Geophysical Research 111, D02110. Cordeiro, R.C., Turcq, P.M., Turcq, B.J., Moreira, L.S., Rodrigues, R.C., Costa, R.L., for reviewing an earlier version of the manuscript. Mário Terra Sifeddine, A., Simões Filho, F.F.L., 2008. Acumulação de carbono em lagos Araújo is also thanked for kindly permitting access to botanical amazônicos como indicador de eventos paleoclimáticos e antrópicos. Oecologia collections of the Six Lakes Hill, Maria de Nazaré C. Bastos and Brasiliensis 12, 130e154. Antonio Elielson Sousa da Rocha for herbarium information and Cordeiro, R.C., Turcq, B., Sifeddine, A., Lacerda, L.D., Silva Filho, E.V., Gueiros, B., Potty, Y.P., Santelli, R.E., Pádua, E.O., Patchinelam, S.R., 2011. Biogeochemical Bruce W. Nelson for collecting the moss sample at the hill. This indicators of environmental changes from 50 ka to 10 ka in a humid region of work was supported by CNPq (processes 575747/2008-0-CT-Ama- the Brazilian Amazon. Palaeogeography, Palaeoclimatology, Palaeoecology 299, e zônia and 477127/2011-8) and by a scholarship awarded to Carlos 426 436. Cowling, S.A., Maslin, M.A., Sykes, M.T., 2001. Paleovegetation simulations of low- D’Apolito. 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