Reconstructing habitats in central Amazonia using megafauna, sedimentology, radiocarbon, and isotope analyses

Quaternary Research 61 (2004) 289 – 300 www.elsevier.com/locate/yqres

Reconstructing habitats in central Amazonia using megafauna, sedimentology, radiocarbon, and isotope analyses Dilce de Fa´tima Rossetti, a,* Peter Mann de Toledo, a Heloı´sa Maria Moraes-Santos, a and Antoˆnio Emı´dio de Arau´jo Santos, Jr. b a b

Museu Paraense Emı´lio Goeldi, Av. Perimetral, 1901, CP 399, CEP 66710-530 Bele´m, PA, Brazil Universidade Federal do Para´, Centro de Geocieˆncias, Campus do Guama´ S/N, Bele´m, PA, Brazil Received 14 November 2002 Available online 30 April 2004

Abstract A paleomegafauna site from central Amazonia with exceptional preservation of mastodons and ground sloths allows for the first time a precise age control based on 14C analysis, which, together with sedimentological and y13C isotope data, provided the basis to discuss habitat evolution within the context of climate change during the past 15,000 yr. The fossil-bearing deposits, trapped within a depression in the Paleozoic basement, record three episodes of sedimentation formed on floodplains, with an intermediate unit recording a catastrophic deposition through debris flows, probably favored during fast floodings. The integrated approach presented herein supports a change in humidity in central Amazonia through the past 15,000 yr, with a shift from drier to arboreal savanna at 11,340 (F50) 14C yr B.P. and then to a dense forest like we see today at 4620 (F60) 14C yr B.P. D 2004 University of Washington. All rights reserved. Keywords: Amazonia; Pleistocene; Paleontology; Mammals; Sedimentology; Radiocarbon dating; Landscape evolution

Introduction Deciphering the origin of the Amazon biodiversity has been a challenge to the scientific community with special interest in issues related to natural history and conservation of communities and ecosystems. An important aspect of this multidisciplinary field is the understanding of the main historical factors relating physical and biological phenomena that acted upon the shaping of the modern biome as we see today. In order to reconstruct the origin and the historical events of the main ecological processes that took place to form the rain forest, an analysis and organization of a series of multidisciplinary data related to geology and climate and a reasonable control of the fossil history are needed. So far, geological and paleontological data are relatively scarce, considering the continental dimensions of the Amazon region, and the information available furnishes only a broad view on the evolutionary patterns. The building of historical datasets is an important contribution to the understanding of * Corresponding author. Fax: (091) 249-0466. E-mail address: [email protected] (D. de Fa´tima Rossetti).

such a large and complex natural system. Although the entire history back to at least the Early Tertiary is relevant to these studies, the Pleistocene should be particularly addressed, as it bears the closest relationship with the modern ecosystem. Only a broad picture of what happened in the Amazon region during the major ecological shifts between ice-age aridity and more humid interglacial periods has been provided so far (reviewed by Latrubesse, 2000). This is mainly due to the following reasons: (1) geological, palynological, and vertebrate paleontological data are still scarce and spotty; (2) information refers only to some areas located in southeastern and southwestern Amazonia; and (3) the best information is related to times before 24,000 yr ago (Latrubesse, 2000). The incomplete information has motivated many debates, with the arid Amazonia refugia model (Haffer, 1969; Prance, 1982) on one side against stability of the forest throughout the Cenozoic on the other side (Colinvaux et al., 2000; Colinvaux and Oliveira, 2001). This paper reports a new fossil quarry bearing two megafauna elements consisting of Haplomastodon waringi and Eremotherium laurillardi from the locality of Itaituba, State of Para´, northern Brazil (Fig. 1), in Central Amazonia,

0033-5894/$ - see front matter D 2004 University of Washington. All rights reserved. doi:10.1016/j.yqres.2004.02.010

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Fig. 1. Location and geologic map of the Itaituba area in the state of Para´, northern Brazil, with the location of the fossil quarry bearing the megafauna of mastodon (Haplomastodon waringi) and giant ground sloth (Eremotherium laurillardi).

which allowed precise age control. Integration of paleontology and sedimentology, as well as radiocarbon and isotope data, provides the basis for discussing the possible changes in this landscape through the past 15,000 yr.

Geological framework and physiography The Itaituba area is located in the southern margin of the Amazonas Basin, which is a large (i.e., nearly 500,000 km2) depression located in the middle and low Amazonas. This basin is bounded by the Guianas Shield to the north, Brazilian Shield to the south, Purus Arch to the west, and Gurupa´ Arch to the east. The origin of the Amazonas Basin is related to rifting associated with intraplate stretching during the

Paleozoic, which took place in three stages and gave rise to a 6500-m-thick sedimentary package represented by three megasequences formed in the Ordovician – early Devonian, middle/late Devonian –early Carboniferous and middle Carboniferous – Permian. The opening of the South Atlantic Ocean and rise of the Andean Cordillera resulted in the tectonic reactivation of the area during the Cretaceous – Cenozoic and deposition of a fourth megasequence up to 500 m thick. This later phase of tectonism continued even in more recent times in the late Quaternary, having a strong effect in the development of the modern drainage system (e.g., Costa and Hasui, 1997; Bemerguy, 1997). The fossil-bearing sedimentary deposits emphasized in this study rest in the left margin of the middle Tapajo´s River and occur overlying limestone of the upper Carboniferous

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Today, the central Amazonia is characterized by a humid to subhumid, equatorial climate, with well-defined dry (June to November) and rainy (December to May) seasons. The registered mean annual precipitation is 2000 mm and the mean temperature is 35j. Vegetation pattern is complex, ranging from dense to open tropical forests, as well as areas of cerrado.

Sedimentology of the fossil beds Facies description

Fig. 2. A view of the Itaituba fossil quarry, illustrating the sharp, erosional contact between the Pleistocene deposits and the underlying Paleozoic Itaituba Formation. Note the karstic structures at the bounding surface (arrows) and the ragged, straight vertical segments of the basement, probably resulting from fault displacement.

Itaituba Formation (Fig. 1). The Tapajo´s River runs through a NE/SW-oriented normal fault zone, which is part of a triple junction formed by strike– slip reactivation of Mesozoic structures during the Quaternary (Costa and Hasui, 1996). This river is in general straight but it becomes highly meandering in the Itaituba region, with large coarse-grained, sandy point bars. The fossil quarry is located in the floodplains, which at this locality reach up to 7 km wide and extend through an area with relief <20 m. A hilly area with Paleozoic rocks displaying altitudes up to 300 m occurs surrounding the floodplains.

The Itaituba megafauna occurs within a thin (<2 m thick) sedimentary package that directly overlies Carboniferous limestone of the Itaituba Formation. A sharp erosional contact occurs between these deposits, forming an unconformity locally marked by a surface with erosional relief of a few meters and with microkarstic structures that form dissolution holes up to 15 cm deep (Fig. 2). The succession with the megafauna also occurs laterally at the same horizontal level as the limestone. In this case, the edge of the Itaituba limestone is defined by a ragged, sharp surface displaying straight, vertical segments (Fig. 2), which suggest fault displacement. Although detailed tectonic studies in the Itaituba area are still unavailable, regional works attest that the Amazon area from Manaus to Bele´m displays a variety of faults formed by a relatively young strike –slip tectonism, which took place during the Miocene/Pliocene and even more recently during the late Pleistocene/Holocene (Bemerguy, 1997; Costa and Hasui, 1996). Three sedimentary successions were distinguished in the Itaituba fossil quarry (Fig. 3). The lowermost unit (unit I) is up to 30 cm thick and rests directly on the basal unconfor-

Fig. 3. Stratigraphy of the Itaituba fossil site, displaying the main characteristic megafauna-bearing sedimentary units formed from late Pleistocene upon a basement with Paleozoic rocks.

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Table 1 List of bone elements of Haplomaston waringi and Eremotherium laurillardi collected from the Itaituba site

H. waringi

E. laurillardi

Cranial elements

Post cranial elements

Isolated molars and fragments of mandible skull Partial skull and jaw fragments of three adult specimens and one newborn individual

Not preserved

Incomplete acropodial, stylopodial, pectoral, and pelvic girdle elements plus several isolated vertebrae and ribs belonging to four individuals (3 adults and 1 newborn). Complete and broken bones are identified as the following: femur, humerus, tibia, fibula, ulna, radius, scapula, pelvis, calcaneum, astragalus, and other bones of the manus and pes.

mity. It consists of a sandy and a light-colored clay facies with a very low content in plant debris. The sandy facies is white to yellowish and comprises well-sorted, fine-grained, massive sands. The overlying clay facies is light gray to greenish and has no observable sedimentary structures. Disarticulated bone fragments of the mastodon H. waringi (Table 1; Fig. 4) were found concentrated at the base of this clay facies. The top of unit I is sharp and defined by vertical, wedge-shaped holes that average 10 cm deep. These cavities were filled with sediments derived from the overlying bed. Grain size analysis shows that the contents of clay and silt fractions in unit I reach up to 86%. Analysis of X-ray diffraction of the clay minerals revealed the presence of smectite, illite, and kaolinite, with the first being by far the dominant one (Figs. 5A and 6). The intermediate unit II averages 1 m thick and consists also of two facies. The lowermost one is represented by poorly sorted, massive conglomerate characterized by quartz and, subordinately, limestone pebbles. Pebbles vary in size, but are usually <3 cm in diameter, and they are sub- to wellrounded. The matrix is composed of mud and a high volume of plant debris, which gives a black color to this facies. Granules and fine- to medium-grained quartz sands are

mixed with the carbonaceous matrix. Ground sloth bones, including several parts of four incomplete E. laurillardi (one newborn and three adults; Fig. 7; Table 1), occur within this facies, being particularly concentrated at its base (Fig. 8). The fossiliferous bed of unit II contains a large amount of wood fragments, with individual logs reaching up to 15 cm long and 3 to 4 cm in diameter. The amounts of both fossils and pebbles decrease upward, which is followed by an increase in the amount of matrix, thus characterizing an overall normal grading. The upper facies in unit II consists of massive, carbonaceous mudstone bearing disperse quartz pebbles and shells, the later sourced from the basement, represented by Paleozoic rocks of the Itaituba Formation. The mudstone displays a lighter color relative to the lower facies of this unit, due to a lower content of carbonaceous debris. Fine-grained quartz sands are dispersed in the mudstone. The contact between the conglomerate and the mudstone in unit II is gradational, and the clay minerals consist of kaolinite and illite, with only minor amounts of smectite (Figs. 5B and 6). The uppermost unit III averages 20– 25 cm thick and consists of black, highly organic mudstone. This unit contrasts with the underlying ones, as it does not contain neither vertebrate fossils nor quartz pebbles, and it is characterized by a high content of organic matter. The clay content is the highest of the whole succession, being represented by up to 95% of the grain sizes. Similar to the underlying units, this succession also shows smectite, illite, and kaolinite, but it is interesting to notice that the relative proportions among these minerals are lower compared to unit I, where smectite clearly dominates (Figs. 5C and 6). Depositional history The Itaituba fossil quarry is located in the central intracratonic Amazon Basin (Fig. 1). It records an area of great stability, without significant sediment preservation since the Paleozoic, when the Itaituba Formation was formed in a shallow marine setting. It is possible that after this time, sedimentation returned to this area only at the end of the Pleistocene, when the sedimentary succession described here was formed. The sharp boundary between these depos-

Fig. 4. Fossils of H. waringi found at the base of unit I in the Itaituba fossil quarry, illustrating (A) a lateral view of a mandible and (B) an occlusal view of a tooth. Scale bar, 5 cm.

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Fig. 5. Results of X-ray analysis of clays from sedimentary units (A) I, (B) II, and (C) III in the Itaituba fossil quarry (I, illite; S, smectite; K, kaolinite).

its and the underlying Paleozoic rocks, forming vertical straight segments, as well as the record of numerous fault traces in the area as indicated by regional studies, suggest that sedimentation might have been renewed due to fault reactivation associated with the late Pleistocene/Holocene phase of strike –slip deformation (Costa and Hasui, 1997). Fault processes would have created traps in the limestone, where the deposits and the megafauna of mammals accumulated. Initially, the rate of fault displacement might have been reduced, creating a shallow depression, where lowenergy sediment deposition took place. During this time (Figs. 9A and 9B), a thin sedimentary succession, represented by unit I, was formed most likely through streams (sandy facies) and then a small lake or pond (clay facies).

The low-energy conditions prevailing in the latter would have been ideal for preservation of the H. waringi remains. The abundance of smectite and illite relative to kaolinite in these beds is suggestive of deposition under climates relatively drier than for the upper units. After lake formation, there was a period of nondeposition, when the lake surface was exposed to a period of subaerial exposure (Fig. 9C), as interpreted from the vertical wedge-shaped holes at the top of unit I, attributed to root development. A renewed period of sediment accumulation took place, forming a thicker succession, represented by unit II. This unit formed under high-flow energy conditions, as indicated by its high volume in quartz pebbles. The lower facies records maximum flow energy when, together with

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Fig. 6. Relative proportions in clay minerals comparing the three sedimentary successions of the study area, based on peak intensity as indicated by the X-ray diffractometers.

the pebbles, a huge amount of vertebrate bones and plant fragments, as well as quartz sands and muds, were all brought together and deposited into the basin as debris flows (Fig. 9D). As flow energy decreased, normal grading was developed. Debris flows occur in most climatic regimes but they are usually initiated in slope areas after heavy rainfall (Leeder, 2001). The four incomplete skeletons of ground sloths, including three adults and a juvenile, mixed with a high volume of other disarticulated bones, suggest accidental death as the most likely, which together with the

Fig. 8. A detail of the base of unit II, with remains of E. laurillardi. Note also abundant quartz pebbles, which decrease in size upward, forming normal grading.

Fig. 7. Examples of fossils of E. laurillardi found in unit II of the Itaituba fossil quarry, illustrating (A) a calcaneum, (B) a dorsal view of a skull from an adult, and frontal views of skulls from (C) an adult and (D) a newborn. Scale bar, 5 cm.

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would be that these debris flows were favored by a combination of fast flooding and fault reactivation, which created space to accommodate the three described sedimentary units. Holocene clay – pebbly conglomerate beds rich in reworked Tertiary fossil vertebrates extensively exposed in western Amazonia have been attributed to a catastrophic flooding resulting from the sudden draining of glacial Lake Titicaca (Campbell and Frayley, 1984; Campbell et al., 1985). Although we do not have evidence to support their model, it is interesting to note that coarse-grained deposits would be expected in such a flooding event and the high amount of quartz pebbles associated with the debris flow deposits from the base of unit II could be a record of such a large-scale phenomenon. However, the data presented in this study are local and allow only speculation about the origin of the flooding event. The upper facies in unit II is also attributed to debris flows, but this deposit differs from the underlying one as it bears a higher amount of matrix, has only dispersed vertebrate fossils, and shows a high content of shell fragments eroded from the Paleozoic basement. These characteristics point to a genesis related to waning flows as the most likely. The high content in plant debris supports a vegetated area, and the prevalence of kaolinite relative to the other clay minerals suggests deposition during a period of higher humidity compared to the underlying stratigraphic unit. The sharp, undulating surface at the top of unit II suggests another period of nondeposition. This was followed by the accumulation of a thin succession, represented by the black clay in unit III. This deposit records the return to basin stability and sediment accumulation in low energy areas of the floodplain, which was then densely vegetated (Fig. 9E). The high amount of organic matter and clay minerals (up to 96%) is consistent with this interpretation. The low proportional difference between smectite and illite relative to kaolinite and the high content in plant debris point to an environment developed under high humidity (e.g., Tucker, 1981; Chanley, 1989).

Radiocarbon dating

Fig. 9. Proposed reconstruction of landscapes for the Itaituba area, as indicated by the depositional units described in this paper. (See text for explanations).

occurrence in the debris flow deposits, is consistent with a catastrophic event. An event such as a flash flooding might have promoted slope instability, death of the ground sloths, and their transportation into the basin together with the other debris. Considering the proposed fault displacement as the origin for this Pleistocene basin, an alternative explanation

Four samples were dated at the Beta Analytic Radiocarbon Dating Laboratory (Table 2). Carbon from samples 1 and 2, corresponding to the Haplomastodon and Eremotherium derived from depositional units I and II, respectively, was extracted from collagen using alkali (NaOH) washes, reduced to graphite (100%C), and dated by accelerator mass spectrometer (AMS). The first sample might include some exogenous carbon within the collected organics due to degradation of bone protein, but sample 2 provided accurate measurement. Samples 2 and 3, corresponding to wood and organic sediments derived from depositional units II and III, respectively, were dated by scintillation spectrometer. The first sample was pretreated with acid to remove carbonates and weaken organic bonds, washed with alkali to remove

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Table 2 Conventional and AMS radiocarbon dates of the Itaituba quarry samples. 14

13

C/12C (x)

Sample

Dep. unit

Type of material

4

III

Wood

4620 (F60)

29.6

3

II

Wood

37,700 (F540)

31.3

2

II

11,340 (F50)

26.9

1

I

Bone collagen Bone collagen

15,290 (F70)

28.5

C yr B.P.

Cal year B.P. 5570 – 5540; 5470 – 5270; 5170 – 5070 Outside the calibration range 13,760 – 13,700; 13,470 – 13,140 18,730 – 17,860

secondary organic acids, and then combined with acid again to provide more accurate dating. Sample 4 was repeatedly washed with acid (HCl) to ensure the absence of carbonates. The 14C results confirm that, during the past 15,000 yr, sedimentation in the Itaituba quarry did not take place as a continuum, but through different episodes of deposition alternated with erosion. The bone fragment of H. waringi collected from unit I was preserved within mud deposits formed in a low-energy setting (i.e., lake or pond) and does not show any evidence for reworking. The age obtained by AMS indicates 15,290 (F70) 14C yr B.P. Despite the possibility that some exogenous carbon might have been added to this sample, given some degradation of the bone protein attributed to subaerial exposure during formation of a discontinuity surface at the top of unit I, the indicated age is consistent with the stratigraphic position of this sample. The two samples from unit II provided very distinctive radiocarbon ages. Hence, sample 2, corresponding to bone material of E. laurillardi, indicated 11,340 (F50) 14C yr B.P, while the wood fragment was dated at 37,700 (F540) 14 C yr B.P. Because the analyzed ground sloth bone came from an articulated specimen, and bone protein was exceptionally well preserved, it is concluded that deposition of unit II took place at 11,340 (F50) 14C yr B.P. The wood sample indicating a much older age was clearly reworked from older deposits underlying the studied sedimentary succession, or from nearby depositional sites, during mass failure through debris flows. Unfortunately, the small pieces of this material did not allow further studies concerning the type of vegetation. Unit III was deposited much more recently, as revealed by radiocarbon analysis of its organic content, indicative of 4620 (F60) 14C yr B.P. These data are consistent with the presence of a discontinuity surface at its base, which is attributed to another period of nondeposition and/or erosion.

y13C isotope data y13C data have been increasingly used as an important tool for reconstructing ancient landscapes regarding C3- and C4-dominated plants. This is possible because, in general the y13C values of C3 and C4 plants range from 26 to

28x and from 12 to 28x, respectively (Merwe, 1982; Tieszen, 1991). This allows making a distinction from forest- to grass-dominated vegetation, an approach that has been used to characterize modern and ancient vegetation patterns (e.g., Merwe and Medina, 1991; Bird et al., 1992; Magnusson et al., 2002; Kastner and Gon˜i, 2003). However, empiric studies have shown a broader range of values, and even overlaps, within plant groups (Medina et al., 1986). For the particular case of Amazonia, depleted values as low as 37x have been recorded for the undergrowth vegetation and 31.5x for the upper canopy (Merwe and Medina, 1991). Stable carbon isotope was measured in materials derived from the three stratigraphic units of the Itaituba site (Table 1). Collagen from H. waringi collected in unit I indicates y13C value of 28.5x. Unit II shows values of 26.9 and 31.3x for collagen from E. laurillardi and the reworked wood fragment, respectively. Organic debris derived from unit III gave a y13C value of 29.6x. Before interpreting these data, the collagen – diet spacing must be considered. In general, the ratio in bulk plants is transferred to higher trophic levels, but the absorption of carbon by the collagen may vary according to metabolic rates, food preferences, body size, and, possibly, phylogenetic distances (e.g., Merwe, 1982; Merwe and Medina, 1991; Tieszen, 1991). The collagen –diet relationship of extinct megafauna can be only estimated. Considering the enrichment of collagen relative to diet for large size browsers of +5.3x (Merwe and Medina, 1991), the isotope data obtained from the Haplomastodon and Eremotherium of the Itaituba site indicate a C3 vegetation corresponding to 33.8 and 32.2x, respectively. Considering these corrections, the y13C values of the Itaituba site, ranging from 28 to 33.8x, indicate the prevalence of C3 plant types in this central Amazonian area at least for some of the past 37,700 yr. That is not to say, however, that a dense forest vegetation would have dominated through this time, as arboreal savannas with more than 40% of tree cover might display y13C values that are undistinguishable from forest values (Merwe, 1982; Magnusson et al., 2002). Taking this into account, the y13C isotope results must be used in integration with geological and paleontological data in order to provide a full discussion of paleolandscapes in the study area, as presented below.

The use of megafauna as a paleoecological indicator Two major points must be taken into account regarding the usefulness of megafauna as past environmental indicators. The first is related to definition of paleoecological variables, such as of broad or specific preferences for open and/or closed habitats. The second is related to the historical control of events, which poses the major restriction in efforts of timing correlation between the different megafauna sites.

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The megafauna association, mostly including large mastodons (Haplomastodon) and ground sloths (Eremotheerium), is common in several Brazilian sites and has been used to support changes from closed to more open habitats during the late Cenozoic in northern South America (Rancy, 1991). Studies based on the analysis of body design led to relate mastodon with a savanna-like environment and Eremotherium with a forest edge (Webb and Rancy, 1996; Rancy, 2000). Based on this information, it has been proposed that such mammals are reliable indicators for reconstructing past Amazon landscapes. However, four main problems must be considered: (1) most of the studies have solely reported the occurrence of taxa, without precise dating; (2) the data available have included only transported fossils along riverbanks, which do not allow one to test the hypotheses on the timing and mode of environmental changes in northern South America; (3) the findings of Pleistocene mammals in the Brazilian Amazon, especially mastodons and ground sloths, are concentrated in the western and southern marginal areas, leaving a void of information about the advance and retreat of open-environment/savanna-like habitats in the central and northern portions of the basin; and (4) findings regarding the combined association of Haplomastodon and Eremotherium have been regarded as a stratigraphical marker for the late Pleistocene/ Holocene (Rancy et al., 1984), which has led interpretations of regional geographical correlation to be so far highly speculative. Furthermore, the use of megafauna elements as habitat indicators (Owen-Smith, 1988) has been questioned on the basis of the statement that large mammals, like tapirs, may develop adaptive capability to different types of landscapes (Colinvaux et al., 2000). In fact, some modern African proboscideans, which are modern counterparts of mastodons, occupy a variety of habitats, including open savanna, wet marsh, thorn bush, semidesert scrub, and even deep forest, and the Asiatic elephant, which also shows large body size, varies in habitat from grassy plains to thick jungles (Nowak, 1999). The wide distribution for such large-size animals, and mostly their record in deep forest habitats, leads us to review the overall assumption that mastodons were actually restricted to savanna-like habitats. However, one must take into account the large difference in sizes among the megafauna associated with the Pleistocene deposits throughout the Amazon, such as ground sloths, mastodons, glyptodonts, pampatheres, toxodons, camelids, large-sized capybaras, and litopterns, which is in great contrast to the small size range of the modern mammals that inhabit the dense Amazon forest, like tapirs and artiodactyls (Webb, 1991; Webb and Rancy, 1996; Rancy, 2000; Croft, 2001). This strongly supports the presence of relatively more arid climate regimes and the existence of large areas with more open, though not necessarily grass-dominated, Pleistocene environments.

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A similar approach is provided in the case of terrestrial sloths. As opposed to mastodons, there is no modern analog for these animals, thus any effort toward ecological reconstructions must rely on its geographical distribution, fauna associations, and inferences from biomechanical information. Eremotherium displays, with the modern puma (Felis concolor), one of the largest latitudinal distributions of a mammalian species in America (Hoffstetter, 1982; Toledo, 1986; Cartelle and de Iullis, 1995). Pleistocene occurrences of this terrestrial sloth are known from southeastern North America to southern Brazil. The other sister taxon, Megatherium, was restricted to southern South America with northern limits at the central portions of the Andean valleys. There is a consensus among most of the authors (e.g., Toledo, 1986; Cartelle, 1999; Webb, 1999) that the large herbivores were mixed feeders and that the pan-American megafauna taxa inhabited a mosaic of savanna with forest patches. The broad latitudinal and altitudinal biogeographic distribution suggests that Eremotherium occupied a wide range of ecological habitats and might have fed on a variety of plant types sourced from gallery forests, open woodlands, and shrub-covered areas. This is particularly suggested on the basis of morphological features of dental patterns and postcrania, which resulted in a combination of a unique body design and large size (up to 6 m in length). Such adaptations include a doubled parallel chisel-like tooth wear pattern adapted for cutting/crushing of foliage, twigs, and possibly fruits; long anterior limbs and large-clawed manus, which were very efficient for branch reaching while displaying a bipedal stance and particularly for defense, avoiding predators in open environments (a frequent incursion in dense forests would increase the vulnerability against ambush predators such as large cats); and long tongues frequently used in the process of food gathering. The hairy and thick skin was adapted for protection against plant structures such as thorns and needles. Such characteristics suggest that these ground sloths were better adapted to open vegetation communities than to dense forests. In addition, paleontological data support that megatheres displayed a gregarious social behavior. This is shown by the Itaituba ground sloths and other findings, such as the one from the Toca dos Ossos in the State of Bahia, central Brazil, where a large number of complete skeletons were recovered from a natural trap cave (Cartelle and Boho´rquez, 1982). These characteristics are strong evidence to discard a closed canopy forest as the preferential habitat of these animals, since group behavior among large mammals in modern habitats is more frequently observed in open habitats. Finally, it has been demonstrated that Eremotherium had a high browser adaptation (Toledo, 1998), as suggested by its giant size, the large claws of the upper members, and the possibility of standing in the upright position.

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Habitat evolution in central Amazonia: an integrated approach Evolutionary models relating to the Amazonian biodiversity are based on the assumption that global climate during the Quaternary was the major driving force of habitat modification, which affected and, at the same time, enhanced the changes in precipitation, depositional/erosional levels, and, ultimately, the geomorphologic framework. Despite a recent proposal favoring a continuous forest cover throughout most of the Amazon region since the mid-Cenozoic (Colinvaux and Oliveira, 2001), a multitude of scientific fields, coming mainly from geology, palynology, genetics, and biogeography, has led to the general acceptance that the Amazonian ecosystem experienced several alternating wet and dry periods, which resulted in forest and savanna expansion, respectively (Mo¨rner et al., 2001; van der Hammen, 2001; Haffer, 2001). Among these data, pollen analysis has been so far the only reliable source from the fossil record, providing information about Pleistocene paleoenvironmental changes in the Amazonia with precise age control (Absy et al., 1991; Sifeddine et al., 2001). However, the pollen record is still scarce and spotty, providing only a broad picture of what happened during the major ecological shifts of glacial and interglacial periods. There are few studies of the Amazonian megafauna with precise stratigraphic control (e.g., Rancy, 1991; Latrubesse and Rancy, 1998). These works have been crucial to support dry periods, with savanna expansion in the western Amazonia. This paper represents the first documentation based on an integrated approach using paleontology, sedimentology, and radiocarbon and isotope data that allow insights into past habitats from the latest Pleistocene in a central Amazonian area. This time was characterized by a worldwide drop in sea surface temperature of 1 – 4j, with the proposed impact in low-latitudinal areas, such as the Amazonia, being represented by several periods of dry climate, with changes in river discharge and sedimentation and development of savanna vegetation (van der Hammen, 2001). The data collected from the Itaituba site do not appear to indicate any drastic landscape changes at least during the past 15,000 yr, although slight variation in vegetation density seems to have taken place through this time. The y13C data, as discussed above, unequivocally discard any significant contribution of tropical grassland savanna vegetation, recording instead a landscape dominated by C3 plants. However, the low content in plant debris observed in the muddy unit I is more consistent with scarce vegetation 15,000 yr ago, suggesting a period with a tendency to aridity. It is interesting to notice that the abundance of smectite relative to the other clay minerals is consistent with an area undergone to low humidity. In addition, although probably not exclusively, Haplomastodon has been preferentially found in association with open paleohabitats.

Based on the combination of these data, we envisage a landscape with arboreal savannas for the study area 15,000 yr ago. It is appropriate to include a brief discussion on the potential paleoenvironmental significance of the wood associated with the fossil sloths. This is because the obtained age of 37,700 14C yr B.P. is close to those from many other Amazonian sites, which have been related to open habitats (e.g., Rasa¨nen et al., 1990; van der Hammen et al., 1992; Latrubesse and Rancy, 1998). As previously mentioned, the wood fragment dated here was reworked from older deposits, being derived either from underlying beds or from nearby depositional sites. In either case, it records a period of sedimentation taking place before deposition of the studied deposits. The y13C value of 31x could suggest a dense forest rather than open habitats in this central Amazon area at 37,700 14C yr B.P., but this interpretation is biased considering the reworking nature of this material and the absence of any further information related to this depositional time. At 11,340 (F50) 14C yr B.P., the landscape seems to have remained similar, though the humidity might have been slightly enhanced. This is suggested by the relative increase in kaolinite relative to other clay minerals in unit II. The high content of logs and plant debris in this unit could also be a further support for the proposed increased humidity. However, the deposits with abundant quartz pebbles attributed to debris flows conform to the presence of open land areas. This information suggests an environment with arboreal savannas similar to the one that occurred at 15,000 yr ago. The presence of E. laurillardi in unit II is consistent with a landscape with abundant trees, as this ground sloth genus had a high browser nature. The possibility of a diet including upper canopy leaves could explain the slightly heavier y13C values of the giant sloths, as in a same area the undergrowth vegetation is usually depleted in y13C relative to the upper canopy (Merwe and Medina, 1991). Finally, as shown in the foregoing discussion, the presence of Eremotherium in these deposits is in itself highly suggestive that a dense forest was not present yet in the Itaituba area around 11,000 yr ago, when open woodlands seem to have dominated the habitat. At 4620 (F60) 14C yr B.P. even moister conditions seem to have prevailed, with the establishment of a forest vegetation similar to that seen today in the Itaituba area. The y13C value of 29.6x for organic soils indicates a C3 tree cover (values obtained from modern Amazon soils are usually less than 27x according to Magnusson et al., 2002). However, the high amount of organic matter and clay minerals, the latter with low proportional difference between smectite and illite relative to kaolinite, is consistent with an environment developed under higher humidity than those recorded for the underlying units. Hence, it is proposed that after sediment deposition through debris flows (unit II), there was a return to low-energy deposition, with development of ponds and/or marshes along floodplains in a

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forested area undergoing higher humidity than in the previous time intervals recorded here. While pollen data from deep-sea fan hemipelagic and continental shelf sediments through the past 50,000 yr support that the Amazon Basin forests were not extensively replaced by savanna vegetation during the glacial period (Heberle and Maslin, 1999; Kastner and Gon˜i, 2003), other sources of information led to the proposal of drastic changes in environmental conditions during this time interval. A wide array of data from different fields of biology and geology has pointed out successive periods of dry and wet climate throughout the Pleistocene and on, which resulted in changes from savanna to rain-forest vegetation. For instance, in a seminal work revising the hypotheses to explain the origin of species in Amazonia, Haffer (2001) has eloquently put strong arguments for drastic changes in climate pattern supported by a large body of hard evidence. In addition, pollen data from the Caraja´s area shows a period of dry climate with savanna vegetation between 25,000 – 10,000 yr ago (Absy et al., 1991) and 22,000 – 13,000 yr ago (Sifeddine et al., 2001). According to these authors, heavy rainfall and high sediment inflow with variable lake levels and low organic carbon seem to have prevailed between 13,000 and 10,000 yr ago, as a result of climates transitioning from arid to humid. From 10,000 to 8000 yr ago there was a relative increase in humidity, which was followed by drier conditions up to 4000 yr ago, when humidity returned, giving rise to development of rain forests (Sifeddine et al., 2001). Studies along the Rio Negro record abundant suspended load, with formation of white water between 14,000 and 4000 yr ago, attributed to increased erosion during relatively more arid conditions (Latrubesse and Franzinelli, 1998). Only after this time there was a change to black waters, characterized by low suspension load and high organic content as we see today. Our integrated analysis supports a progressively increased humidity in the Itaituba area through the past 15,000 yr, which was directly reflected by a simultaneous change in vegetation cover from arboreal savanna to dense rain forest as we see today. These data add new insights to the discussion of Amazonian climate and landscape during the Quaternary, an issue still largely controversial.

Final remarks The available historical data related to climate evolution throughout the Pleistocene and Recent in the Amazon region are still insufficient to provide a detailed characterization of all shifting episodes. There seems to be an overall fairly good agreement on the major climatic patterns when data from the study area are compared with those from other places located thousands of kilometers apart throughout northern South America, with a change from arid to relatively more humid conditions in the past 15,000 yr. However, the data from the Itaituba area do not reveal any drastic

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change in landscape in central Amazonia. Instead, integration of geological, paleontological, and isotope data revealed only a slight change in humidity and, as a result, vegetation density, with a shift from arboreal savanna to forest. Such interpretation can be easily accommodated with the data obtained from Amazon deep sea fan sediments (e.g., Heberle and Maslin, 1999; Kastner and Gon˜i, 2003), as arboreal savanna would show y13C values that might be indistinguishable from those of forest vegetation. The information provided in this paper should be taken as an additional source of data in the design of large-scale climatic scenarios, but a word of caution must be considered in the interpretations, as the modern landscape in the Central Amazoˆnia area is complex, with open and dense forest and even areas with savannas.

Acknowledgments We acknowledge the support given by Dr. Ima Ce´lia Vieira as the chair-in-charge of the Goeldi Museum during the initial fieldwork. We thank Mr. Antoˆnio Anildo Aguiar and Mr. Joelson Aguiar, who first reported the fossil occurrence on their farm, geologists Every Aquino (DNPM) and Elias Lea˜o Moraes (SEMMA) for field assistance, and to Dr. Walter Neves (USP) for payment for one 14C analysis. Finally, we thank two anonymous reviewers for comments that improved this paper significantly.

References Absy, M.L., Cleef, A., Fournier, M., Martin, L., Servant, M., Sifeddine, A., Ferreira da Silva, M.F., Soubie`s, F., Suguio, K., Turcq, B., van der Hammen, T., 1991. Mise en e´vidence de quatre phases d’ouverture de la foreˆt dense dans leˆ sud-est de l’Amazonie au cours deˆs 60.000 denie`res anne´es. Premie`re comparaison avec d’autres regions tropicales. ´ cade´mie des Sciences Paris 312, 673 – 678. Comptes Rendus de l’A Bemerguy, R.L. (1997). Morfotectoˆnica e evolucß a˜o paleogeogra´fica da regia˜o da calha do rio Amazonas. Ph.D. thesis, Universidade Federal do Para´, Bele´m. Bird, M.I., Fyfe, W.S., Pinheiro-Dick, D., Chivas, A.R., 1992. Carbon isotope indicators of catchment vegetation in the Brazilian Amazon. Global Biogeochemical Cycles 6, 293 – 306. Campbell, K.E., Frayley, C.D., 1984. Holocene flooding and species diversity in southwestern Amazonia. Quaternary Research 21, 369 – 375. Campbell, K.E., Frailey, C.D., Arellano-L., J., 1985. The geology of the Rio Beni: further evidence for Holocene flooding in Amazonia. Contributions in Science – Natural History Museum of Los Angeles 364, 1 – 18. Cartelle, C., 1999. Pleistocene mammals of the Cerrado and Caatinga of Brazil. In: Eisenberg, J., Redford, K.H. (Eds.), Mammals of the Neotropics. The Central Neotropics: Ecuador, Peru, Bolivia, Brazil, 3rd ed. Univ. of Chicago Press, Chicago, pp. 27 – 46. Cartelle, C., Boho´rquez, G.A., 1982. Eremotherium laurillardi (Lund, 1842). 1. Determinacß a˜o especı´fica e dimorfismo sexual. Iheringia 7, 45 – 63. Cartelle, C., de Iullis, G., 1995. Eremotherium laurillardi: the Panamerican late Pleistocene megatheriid sloth. Journal of Vertebrate Paleontology 15, 830 – 841. Chanley, H., 1989. Clay Sedimentology Springer-Verlag, Berlin.

300

D. de Fa´tima Rossetti et al. / Quaternary Research 61 (2004) 289–300

Colinvaux, P.A., Oliveira, P.E., 2001. Amazon plant diversity and climate through the Cenozoic. Palaeogeography, Palaeoclimatology, Palaeoecology 166, 51 – 63. Colinvaux, P.A., Oliveira, P.E., Bush, M.B., 2000. Amazon and Neotropical plant communities on glacial time scales: the failure of the aridity and refuge hypotheses. Quaternary Science Reviews 19, 141 – 169. Costa, J.B.S., Hasui, Y., 1997. Evoluc¸a˜o Geolo´gica da Amazoˆnia. In: Costa, M.L., Ange´lica, R.S. (Eds.), Contribuic¸o˜es a` Geologia da Amazoˆnia. Falaˆngola, Bele´m, pp. 16 – 76. Croft, D.A., 2001. Cenozoic environmental change in South America as indicated by mammalian body size distributions (cenograms). Diversity and Distributions 7, 271 – 287. Haffer, J., 1969. Speciation in Amazonian forest birds. Science 165, 131 – 137. Haffer, J., 2001. Hypotheses to explain the origin of species in Amazonia. In: Vieira, I.C.G., Silva, J.M.C., Oren, D.C, D’Incao, M.A. (Eds.), Diversidade Biolo´gica e Cultural da Amazoˆnia. Editora do Museu Paraense Emı´lio Goeldi, Bele´m, pp. 45 – 118. Heberle, S.G., Maslin, M.A., 1999. Late Quaternary vegetation and climate change in the Amazon Basin based on a 50,000 year pollen record from the Amazon Fan, ODP Site 932. Quaternary Research 51, 27 – 38. Hoffstetter, R., 1982. Les e´dente´s xe´narthres, un groupe singulier de la faune ne´otropicale: origine, affinite´s, radiation adaptative, migrations et extinctions. In: Gallitelli, M. (Ed.), Proceedings of the First International Meeting on Paleontology, Essential of Historical Geology. Societa` Tipografica Editrice Modenese Mucchi, Modena, Italy, pp. 385 – 443. Kastner, T., Gon˜i, M.A., 2003. Constancy in the vegetation of the Amazon Basin during the late Pleistocene: evidence from the organic matter composition of Amazon deep sea fan sediments. Geology 31, 291 – 294. Latrubesse, E.M., 2000. The late Pleistocene in Amazonia: a paleoclimatic approach. In: Smolka, P., Volkheimer, W. (Eds.), Southern Hemisphere and Neoclimates. Springer-Verlag, Germany, pp. 209 – 224. Latrubesse, E.M., Franzinelli, E., 1998. Late Quaternary alluvial sedimentation in the upper Rio Negro Basin, Amazoˆnia, Brazil: paleohydrological implications. In: Benito, G., Baker, V.R., Gregory, K.J. (Eds.), Paleohydrology and Environmental Change. Wiley, Germany, pp. 261 – 271. Latrubesse, E.M., Rancy, A., 1998. The late Quaternary of the upper Jurua´ River, southwestern Amazonia, Brazil: geology and vertebrate paleontology. Quaternary of South America and Antarctic Peninsula 11, 27 – 46. Leeder, M., 2001. Sedimentology and Sedimentary Basins—from Turbulence to Tectonics, 2nd ed. Blackwell Sci., Oxford. Magnusson, W.E., Sanaiotti, T.M., Lima, A.P., Martinelli, L.A., Victoria, R.L., Arau´jo, M.C., Albernaz, A.L., 2002. A comparison of y13C ratios of surface soils in savannas and forests in Amazonia. Journal of Biogeography 29, 857 – 866. Medina, E., Montes, G., Cuecas, E., Rokzandic, Z., 1986. Profiles of CO2 concentration and y13C values in tropical rain forests of the upper Rio Negro basin, Venezuela. Journal of Tropical Ecology 2, 207 – 217. Merwe, N.J., 1982. Carbon isotopes, phytosynthesis, and archaeology. American Scientist 70, 596 – 606.

Merwe, N.J., Medina, E., 1991. The canopy effect, carbon isotope rations and foodwebs in Amazonia. Journal of Archaeological Science 18, 249 – 259. Mo¨rner, N.-A., Rossetti, D.F., Toledo, P.M., 2001. The Amazonian rainforest: only some 6 – 5 million years old. In: Vieira, I.C.G., Silva, J.M.C., Oren, D.C, D’Incao, M.A. (Eds.), Diversidade Biolo´gica e Cultural da Amazoˆnia. Editora do Museu Paraense Emı´lio Goeldi, Bele´m, pp. 3 – 18. Nowak, R.M., 1999. Walker’s Mammals of the World, 6th ed. Johns Hopkins Press, Baltimore. Owen-Smith, R.N., 1988. Megaherbivores. The Influence of Very Large Body Size in Ecology. Cambridge Univ. Press, Cambridge, UK. Prance, G.T., 1982. Forest refuges: evidence from woody angiosperms. In: Prance, G.T. (Ed.), Biological Diversification in the Tropics. Columbia Univ. Press, New York, pp. 137 – 158. Rancy, A. (1991). Pleistocene mammals and palaeoecology of the western Amazon. Ph.D. thesis, Univ. of Florida, Gainesville. Rancy, A., 2000. Paleoecologia da Amazoˆnia. Megafauna do Pleistoceno. Universidade Federal de Santa Catarina Press, Santa Catarina, Brazil. Rasa¨nen, M., Salo, J.S., Jungnert, H., Pitman, R., 1990. Evolution of western Amazon lowland relief: impact of Andean foreland dynamics. Terra Nova 2, 320 – 332. Sifeddine, A., Marint, L., Turcq, B., Volkmer-Ribeiro, C., Soubie`s, F., Cordeiro, R.C., Suguio, K., 2001. Variations of the Amazonian rainforest environment: a sedimentological record covering 30,000 years. Palaeogeography, Palaeoclimatology, Palaeoecology 168, 221 – 235. Tieszen, L.L., 1991. Natural variations in the carbon isotope values of plants: implications for archaeology, ecology, and paleoecology. Journal of Archaeological Science 18, 227 – 248. Toledo, P.M. (1986). Descricß a˜o do sincraˆnio de Eremotherium laurillardi (Lund, 1842): taxonomia e paleobiogeografia. M.S. thesis. Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil. Toledo, P.M., 1998. Locomotory Patterns within the Pleistocene Sloths. Museu Paraense Emı´lio Goeldi Press, Bele´m. Tucker, M.E., 1981. Sedimentary Petrology: An Introduction to the Origin of Sedimentary Rocks. Blackwell Sci., Oxford. van der Hammen, T., 2001. Paleoecology of Amazonia. In: Vieira, I.C.G., Silva, J.M.C., Oren, D.C, D’Incao, M.A. (Eds.), Diversidade Biolo´gica e Cultural da Amazoˆnia. Editora do Museu Paraense Emı´lio Goeldi, Bele´m, pp. 19 – 44. van der Hammen, T., Duivenvoorden, J.F., Lips, J.M., Urrego, L.E., Espejo, N., 1992. The late Quaternary of the middle Caqueta´ area (Colombian Amazonia). Journal of Quaternary Sciences 7, 45. Webb, S.D., 1991. Ecogeography and the Great American Interchange. Paleobiology 17, 266 – 280. Webb, S.D., 1999. Isolation and interchange: a deep history of South American mammals. In: Eisenberg, J., Redford, K.H. (Eds.), Mammals of the Neotropics. The Central Neotropics: Ecuador, Peru, Bolivia, Brazil, 3rd ed. Univ. of Chicago Press, Chicago, pp. 13 – 19. Webb, S.D., Rancy, A., 1996. Late Cenozoic evolution of neotropical mammal fauna. In: Jackson, J.B.C., Budd, A.B., Coates, A.G. (Eds.), Evolution and Environment in Tropical America. Univ. of Chicago Press, Chicago, pp. 335 – 358.