NINETEEN The origin of the modern Amazon rainforest: implications of the palynological and palaeobotanical record

Carlos Jaramillo1, Carina Hoorn2, Silane A.F. Silva3, Fatima Leite4, Fabiany Herrera1, Luis Quiroz5, Rodolfo Dino6 and Luzia Antonioli7 1Smithsonian Tropical Research Institute, Balboa, Republic of Panama 2University of Amsterdam, The Netherlands 3Instituto Nacional de Pesquisas da Amazonia-INPA, Manaus, Brazil 4University of Brasília, Brazil 5Smithsonian Tropical Research Institute, Balboa, Republic of Panama, and University of Saskatchewan, Canada 6Cidade Universitária – Ilha do Fundão, Rio de Janeiro, Brazil 7Universidade Estadual do Rio de Janeiro (UERJ), Rio de Janeiro, Brazil

Abstract

Northern South America harbours a highly diversifi ed forest vegetation. However, it is not clear when this remarkable diversity was attained and how it was produced. Is the high diversity the product of a positive speciation–extinction balance that accumulated species over long time periods, or is it the product of high origination rates over short time periods, or both? Middle Cretaceous fl oras, although very poorly studied, are dominated by non-angiosperm taxa. By the Paleocene, pollen and macrobotanical fossils suggest that the basic phylogenetic composition and fl oral physiognomy of Neotropical rainforests were already present. Hence there was a profound change in Amazonian fl ora during the Late Cretaceous, that still needs to be documented. Levels of Paleocene diversity are much lower than those of modern tropical rainforests. By the Early Eocene, however, pollen diversity was very high, exceeding values of modern rainforests. At the Eocene- Oligocene a major drop in diversity coincided with an episode of global cooling. The palynological and palaeobotanical records of Amazonia suggest that high levels of diversity existed during the Miocene, a period when the boundary conditions for sustaining a rainforest (e.g. low seasonality, high precipitation, edaphic het- erogeneous substrate) were met. The predecessor of the present rainforest was formed during the Paleogene and Neogene when the western Amazon lowlands were affected by Andean tectonism, which radically changed drainage systems and promoted wetland development. An overall global cooling during the Neogene also may have affected the rainforest, decreasing its area and expanding adjacent savanna belts. Recent events like the Quaternary ice ages also played a role in the forest dynamics and composition, although it seems to have been minor. In this chapter we will review the main characteristics of the Neogene palynological and palaeobotani- cal records in Amazonia, and we will make some comparisons with pre- and post-Neogene records. The data indicate that the Amazonian rainforest is more likely to be a product of a dynamic geological history stretching back over the past 25 million years rather than the last few hundred thousand years.

Amazonia, Landscape and Species Evolution: A Look into the Past, 1st edition. Edited by C. Hoorn and F.P. Wesselingh. © 2010 Blackwell Publishing

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Introduction Palynology

The Cretaceous and Cenozoic history of the Neotropical rain- Cretaceous Amazonia forest is still not well understood. Very few studies of Cretaceous Amazonian fl oras have been done. Most of the Cretaceous stud- Cretaceous sequences of intracratonic Brazilian basins are mostly ies have been carried out in the eastern margin of South America characterized by terrestrial siliciclastic rocks (see Chapters 3 & 7), (e.g. Herngreen 1973, 1975; Regali et al. 1974; De Lima 1979), and which often give a poor yield of palynomorphs. The Cretaceous most of them have focused on palynology. Alter do Chão Formation forms the basal unit of the Javari Group, Paleogene records, mainly deriving from northern South which represents the beginning of the fi nal sedimentation episode America, show that a rainforest with family-level fl oristic com- in the Amazonas and Solimões Basins. Fossils are rare in the pre- position and leaf physiognomy similar to modern Neotropical dominantly fl uvial Alter do Chão Formation and limited to single rainforests already existed by the Middle Paleocene (Wing fi ndings. Price (1960) found a terapode tooth in the upper part et al. 2004; Doria et al. 2008; Herrera et al. 2008a). However, of the formation in the 1-NO-1-AM well in the Amazonas Basin. its diversity was much less than modern lowland Neotropical Daemon & Contreiras (1971) dated the formation as Cenomanian rainforests (Wing et al. 2004; Jaramillo et al. 2007a). The be- to Maastrichtian, based on the correlation with the K-400-K-600 ginning of the Eocene shows a very rapid increase in diversity palynozones defi ned in the Barreirinhas Basin by Lima (1971). and the radiation of several Neotropical plant families. Levels They also mentioned the occurrence of teeth and fragments of of diversity by the Middle Eocene were greater than those of vertebrates in the upper part of the formation. modern Amazonian forests (Jaramillo et al. 2006). Eocene paly- Daemon (1975) analysed the palynology of two wells that drilled nofl oras contain a large number of pollen taxa that range into the formation (1-NO-1-AM and 1-AC-1-AM), and esta blished an the Neogene and are more similar to each other than to the early Albian to early Cenomanian age for the lower part of the for- Paleocene palynofl oras. At the Eocene-Oligocene boundary a mation, and a late Cenomanian to Turonian age for the middle part. marked decrease in diversity occurred, and the number of pol- The upper part remained undated. The age was given by correlation len taxa fell below modern levels. This drop correlates with a with the palynostratigraphic scheme of Lima (1971) and Herngreen major global cooling and the beginning of the Antarctic glacia- (1973) for the Barreirinhas Basin. Dino et al. (1999) studied 43 core tion (Jaramillo et al. 2006). samples from the Alter do Chão Formation in 1-NO-1-AM and The Neogene was a period characterized by a changing climate, 9-FZ-28-AM wells (Fig. 19.1). They described two sequences in the fl uctuating sea levels and tectonic instability (Zachos et al. 2001). formation. The predominantly sandy lower sedimentary sequence These three phenomena all left their mark in the Amazonian land- was formed during the late Aptian-Albian from terrigenous infl uxes scape and its vegetation development (see Chapter 26). Although fed by cycles of anastomosing fl uvial systems with secondary aeo- the Neogene sedimentary record is incomplete, outcrops along lian reworking. At the base, unconformably overlying the Andirá the rivers and well data obtained through mineral exploration Formation, there are meandering deposits with abandoned channels together have provided us with an insight into the vegetational fi lled with clay. Those clays are rich in vegetal, amber fragments, root history. prints, fi sh remains, freshwater ostracods and conchostracan frag- The record of plant diversity in the Amazons is still incomplete. ments. The upper sequence accumulated during the Cenomanian. Nevertheless, palynological and palaeobotanical data reveal that It is almost entirely composed of fi ne-grained sediments that are during the Neogene Amazonia already was covered by a highly interpreted to represent fl uvial-deltaic-lacustrine settings. diversifi ed and multistratifi ed forest that varied in composition Dino et al. (1999) identifi ed two distinct palynofl oras (see and distribution over time under the infl uence of the major Fig. 19.1). Characteristic pollen and spores from the late Aptian- events (Hoorn 1993, 1994a, 1994b, 2006). The potential effect Albian palynofl ora (from the lower sequence) and the Cenomanian on Amazonian forests of global cooling and possible associated fl ora from the upper sequence are listed in Tables 19.1& 19.2. changing precipitation patterns over the last 5 million years is The Cretaceous vegetation was completely dominated by non- unclear. Preliminary evidence suggests a major reduction in angiosperm taxa (ferns and gymnosperms), with very few angio- area from that formerly covered by rainforest. Areas in northern sperms, unlike modern tropical forests, which are populated chiefl y Venezuela (e.g. Urumaco in Falcon Dept.) that were fl oristically by angiosperms (Gentry 1982).The presence of large numbers of similar to Amazonia during the Late Miocene, became isolated by spores, pollen grains and woody fragments of terrestrial origin, as the rise of the Andes and subsequently underwent a transforma- well as the absence of marine elements, suggests a strong continen- tion to dry vegetation. There was also an extensive development tal infl uence during the deposition of the Cretaceous Alter do Chão of tropical savannas, that further encroached on the Amazonian Formation. The low frequency of palynomorphs produced by plants rainforest. The overall effect of this reduction in forested area on better adapted to dry climates (e.g. Classopollis, Equisetosporites and Amazonian vegetation is unclear, but it might have caused a loss Gnetaceaepollenites) suggests that the Alter do Chão Formation was in diversity. However, it is now evident that the Quaternary gla- not deposited under arid climatic conditions. cial cycles did not signifi cantly affect diversity in Amazonia (Bush 1994; Rull 2008; see also Chaper 20). Amazonian Holocene cores do not show a signifi cant change in diversity or fl oristic compo- Paleogene northern South America sition. Furthermore, most of the species dated using molecular techniques indicate origination ages older than 2 million years Tropical Paleogene palynology of tropical South America has been ago (Rull 2008). widely researched since the 1950s (Van der Hammen 1954, 1956a,

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63º 30' 57º 30' 51º 30'

1º 00' 1º 00'

1-AC-1-PA

North Platform 9-FZ-28-AM 1-NO-1-AM Central Trough 3º 00' 3º 00' 2-MD-1-AM

os SOUTH HINGE South Platform 5º 00' 5º 00'

63º 30' 57º 30' 51º 30'

A B C

Fig. 19.1 Locations of the wells analysed and key palynomorphs found in the Cretaceous Alter do Chão Formation. (a) Triorites africaensis; (b) Galeacornea causea; (c) Elateroplicites africaensis.

Table 19.1 Characteristic pollen and spores of the late Table 19.2 Characteristic pollen and spores of the Aptian-Albian palynoflora from the lower sequence of the Cenomanian palynoflora from the upper sequence of the Brazilian Alter do Chão Formation. Brazilian Alter do Chão Formation.

Araucariacites australis Classopollis alexi A. guianensis Elateroplicites africaensis (with two appendages) Afropollis jardinus Galeacornea causea Callialasporites dampieri Gnetaceaepollenites similis Cicatricosisporites avnimelechi G. crassipolli Classopollis alexi G. clathratus Crybelosporites pannuceus Psilastephanosporites brasiliensis Cyathidites australis Triorites africaensis Dictyophyllidites harrisii Equisetosporites ambiguus 1956b, 1957a, 1957b, 1958; Van der Hammen & Wymstra 1964; Van Exesipollenites tumulus Hoeken-Klinkenberg 1964, 1966; Van der Hammen & García 1966; Gonzalez-Guzman 1967; Germeraad et al. 1968; Doubinger 1973, Inaperturopollenites simplex 1976; Regali et al. 1974; Van der Kaars 1983; Guerrero & Sarmiento Klukisporites variegatus 1996; Jaramillo & Dilcher 2000, 2001; Jaramillo 2002; Jaramillo Sergipea variverrucata et al. 2005a, 2005b, 2007a; Pardo-Trujillo et al. 2003; Jaramillo & S. simplex Rueda 2004; Santos et al. 2008), and an electronic morphologi- cal database (Jaramillo & Rueda 2008) has been compiled. About Spheripollenites scabratus 450 fossil species have been named. Most of the work has been

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done in Colombia, Venezuela and coastal areas of Brazil. The overall Formation contains abundant fossiliferous levels with vertebrate, palynofl ora shows a fl uctuation in forest diversity that correlates invertebrate and plant remains (e.g. Maia et al. 1977; Latrubesse with global temperatures. Diversity increased in periods of glo- et al. 2007; see also Chapters 15–18). Outcrop samples generally bal warming and decreased during global cooling (Jaramillo et al. give a very good snapshot of palaeovegetation and its diversity. 2006). Published data also suggest the absence of extensive savan- Outcrops in the Amazon often occur far apart from each other, do nas and a more regional extent of the Amazonian forest reach- not extend beyond 60 m of vertical exposure, and their strata have ing northern Colombia and Venezuela (Jaramillo 2002), possibly low dipping angles. Therefore it is diffi cult to correlate between also the result of the slightly more southerly location of the South outcrops and establish their relative age. Core material offers a American continent, which resulted in the region being several complementary view of the Amazonian Neogene by obtaining degrees closer to the Equator (Pardo-Casas & Molnar 1987). more complete stratigraphic successions that may not be available Paleogene fl oras lack the Asteraceae and have low abundances in outcrops. of Poaceae, which are very common in many Neogene tropical A series of exploration wells were drilled in Amazonia during South American fl oras. Eocene fl oras also seem to have been more the 1970s (Maia et al. 1977) and remained stored in the Geological diverse than Early Miocene fl oras (Jaramillo et al. 2006). Service of Brazil Manaus offi ces (Brazil). These wells have pro- The Paleogene record from the present-day Amazonian region vided an initial biostratigraphic framework (Hoorn 1993) and are is virtually undocumented due to the absence of outcrops of this currently the subject of further study. The Neogene succession age and because this interval has not yet been studied in available in Amazonia is very condensed, in about 300–600 m of vertical cores. Future studies can address this issue by looking at exposed section, making the study of these sediments a complex problem deposits in the sub-Andean zone and Andes of Peru, Bolivia and because of both condensation and hiatuses. Ecuador. Well data permit a subdivision into palynological zones, which have been correlated to Caribbean zonations (Germeraad et al. Neogene Amazonia 1968; Lorente 1986) that have been calibrated with nanoplankton and foraminifera (Muller et al. 1987). The existing biozonation Palynological sampling locations, lithologies and for Amazonia (Hoorn 1993) is complemented with more recent processing methods well data from Late Miocene and Pliocene intervals, as shown in Fig. 19.2. The margins of the Amazonian rivers and their overbanks are Hoorn (1993) defi ned fi ve palynological zones in northwestern mostly covered by lush rainforest with a predominance of taxa Amazonia: such as Cecropia, Mauritia and Malvaceae. Occasionally, the densely forested river margins provide a glimpse of the Neogene 1 Verrutricolporites Acme Zone (Early Miocene); record that forms a signifi cant part of the Amazonian subsurface. 2 Retitricolporites Acme Zone (Early Miocene); These sediments provide us with an insight into past deposition- 3 Psiladiporites-Crototricolpites Concurrent Range Zone (late al environments and are suitable for palynological analysis and Early to early Middle Miocene); palaeovegetation reconstructions. 4 Crassoretitriletes Interval Zone (Middle Miocene); The most productive sediments for palynological sampling 5 Grimsdalea Interval Zone (late Middle-early Late Miocene). are organic-rich clays, lignites and siltstone, which are often intercalated in the fl uvial and lacustrine sequences. A detailed These zones were established using the palynological information impression of the vegetation development in a fl uvial system over of 54 samples from two wells: 1AS-4a-AM (04°23´S, 70°55´W) time can be obtained by sampling at small intervals of c. 10 cm. and 1AS-51-AM (01°51´S, 69°02´W) and were correlated with Subsequently these samples then should be processed in the assemblages described by Lorente (1986) for northern Venezuelan laboratory, depending on their lithology, consolidation and pres- sedimentary basins. ence of calcium carbonate. As palynological particles behave as Recent palynological studies have found two additional, sediment particles, a concentration of larger or smaller fragments younger zones in northwestern Amazonian sediments (Silva may result, depending on the technique used (Leite 2006). In some et al. in press), the Asteraceae- Fenestrites zone and Psilatricolporites studies a clay defl occulating technique was used (Hoorn 1993, caribbiensis zone of Lorente (1986). The most important species 1994a, 1994b, 2006) whereas other studies applied hydrofl uoric for each zone are illustrated in Fig. 19.2, and an overview of taxa acid (HF) (Rebata et al. 2006; Latrubesse et al. 2007) or a combi- is provided in Table 19.3. nation of HF and decantation. When different processing tech- niques are used, i.e. including different mesh sizes for separating larger and smaller fragments and decanting, the palynological The Neogene Amazonian fl uvial landscape and the effect results may be different and, consequently, diffi cult to compare. of episodic marine incursions

Early to early Middle Miocene Biostratigraphy Mangrove fl oras dominated eastern Amazonia near Belen (Leite Miocene sediments in western Amazonia are known as Pebas 2004), while fl uvial systems of local origin prevailed in western Formation (in Peru) and Solimões Formation in Brazil but also the Amazonia (Hoorn 1994a), and scattered lacustrine settings existed deposits extend into Colombia and Ecuador. The Pebas/Solimões near the incipient Andean Eastern Cordillera (Gomez et al. 2009).

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3 2 1 (1968) et al. (1987)

et al. Biostratigraphic markers Ma 1 Muller Lorente (1986) Nanoplankton zones zones Planktonic foraminifera Germeraad

2 NN18 NN17 Echitricolporites Echitricolporites Echitiricolporites- mcneylli mcneylli Alnipollenites 3 NN16 N20/21 Alnipollenites verus Echitricolporites mcneillyi 4 NN15/ Psilatricolporites

PLIOCENE NN13 N19 5 caribbiensus NN12 N18 6 Pachydermites diederixi

NN11 Stephanocolpites Fenestrites longispinosus Fenestrites 7 MESSINIAN N17 evansii Pachidermites Echitricolporites Fenestrites spinosus Stephanocolpites evansii diederixi spinosus 8

9 LATE NN10 Asteraceae N16 Hoorn (1993) Psilatricolporites caribbiensis Echitricolporites spinosus 10

TORTONIAN NN9 N15 Fenestrites longispinosus NN8 11 Grimsdalea Grimsdalea Grimsdalea N14 magnaclavata NN7 N13 12 Multimarginites vanderhammenii NN6 N12 Crassoretitriletes Crassoretitriletes Crassoretitriletes 13 vanraadshoovenii SERRAVAL. N11 Grimsdalea magnaclavata 14 N10 NN5 N9 Psiladiporites MIDDLE 15 minimus Multimarginites vanderhammenii Crassoretitriletes vanraadshooveni

MIOCENE Echitricolporites

LANGHIAN Psiladiporites maristellae- Psiladiporites – 16 N8 Psiladiporites Crototricolpites NN4 minimus 17 N7

Psiladiporites minimus Echitricolporites maristellae m 18 NN3 N6 ␮ Retitricolporites Crototricolpites sp. 50 19

BURDIGALIAN Verruticolporites N5 Jandufouria rotundiporus- seamrogiformis Verrutricolporites 20 Echidiporites EARLY NN2 barbeitoensis Verrutricolporites Verrutricolporites rotundiporus 21

22 N4

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4 Fig. 19.2 Most important palynostratigraphic zonations for the South American tropics (modifi ed from Leite 2006), and some of the key taxa used in the / 2

0 zonations. 0 9

1 : 5 7 : 0 0

S h o b h a HHoorn_ch19_Final.indd 322 o o r n _ c h 1 9 _ F i n a l . i n Table 19.3 Summary of the palynomorph species described for the Neogene of Amazonia and their natural affinities. d d

3 2

2 Pollen/spores Amazonia Taxonomic affi nity Ecology Author* (Neogene)

Bacutriletes spp. Selaginellaceae Montane and lowland forest Van der Hammen 1956 ex Potonie 1956 Bombacacidites araracuarensis Bombacaceae, Ceiba Rainforest and marsh forest, lowland Hoorn 1994a Bombacacidites baculatus Bombacaceae, Pachira aquatica Rainforest and mixed swamp Muller et al. 1987 Bombacacidites baumfalkii Bombacaceae Lowland forest, along creeks and rivers Lorente 1986 Bombacacidites nacimientoensis Bombax Lowland forest, along creeks and rivers (Anderson, 1960); Elsik, 1968 Bombacacidites muinaneorum Bombacopsis Lowland forest, along creeks and rivers Hoorn 1993 Bombacacidites spp. Bombacaceae Lowland forest, along creeks and rivers Couper 1960 Clavainaperturites clavatus Croton? Van der Hammen & Wijmstra 1964 Clavainaperturites microclavatus Chloranthaceae, Hedyosmum Montane and lowland forest Hoorn 1994b Clavamonocolpites sp. Palmae, Iriartea Lowland and pre-montane forest Gonzalez-Guzman 1967 Clavatriletes spp. Selaginellaceae? Regali et al. 1974 Corsinipollenites oculusnoctis Onagraceae, Ludwigia Swamps (Thiergart 1940); Nakoman 1965 Crassiectoapertites columbianus Leguminosae, Papilionoideae Lowland forest Dueñas 1980 Crassoretitriletes Schizaceae, Lygodium microphyllum Marshes and swamps Germeraad et al. 1968 vanraadshoovenii Cricotriporites guianenesis Leidelmeyer 1966 Crototricolpites annemariae Euphorbiaceae, Croton Lowland and montane forest Leidelmeyer 1966 Cyperaceaepollis Cyperaceae Savannas and swamps Krutzsch 1970 Cyatheacidiites spp. Cyatheacea Montane region Cookson 1947 ex Potonie 1956 Deltoidospora adriennis Pteridaceae, Acrostichum aureum Close to mangrove vegetation (Potonie & Gelletich 1933) Frederiksen 1973 Echidiporites barbeitoensis Palmae, Korthalsia ferox Lowland forest Muller et al. 1987 Echinosporis spp. Thelypteraceae-Athyriaceae-Marathiaceae Krutzsch 1967 Echiperiporites spp. Malvaceae Van der Hammen & Wymstra 1964 Echiperiporites akanthos Van der Hammen & Wijmstra 1964 Echiperiporites estelae Malvaceae-Convolvulaceae Coastal vegetation Germeraad et al. 1968 Echitricolporites mcneillyi Asteraceae Open vegetation Germeraad et al. 1968 Echitricoloporites spinosus Asteraceae Open vegetation Germeraad et al. 1968 Echitricolporites maristellae Bombacaceae-Malvaceae Lowland forest Muller et al. 1987 Echitriletes cf. muelleri Selaginellaceae? Regali et al. 1974 Ephedripites renzonii Araceae, Spatiphyllum Herbs and epiphytes Dueñas 1986 Ephedripites sp. Ephedraceae Dry forest Bolkhovitina 1953 Fenestrites spinosus Asteraceae Van der Hammen 1956 ex Lorente, 1986 Foveotriletes ornatus Regali et al. 1974 110/24/2009 1:57:02 Shobha 0 / 2 4 / 2 0 0 9

1 : 5 7 : 0 2

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3 2 3 Grimsdalea magnaclavata Palmae Germeraad et al. 1968 Heterocolpites incomptus Melastomataceae, Miconia? Common in Mauritia understorey (Amazonia) Van der Hammen 1956 ex Hoorn 1993 Heterocolpites rotundus Combretaceae-Melastomataceae Hoorn 1993 Heterocolpites verrucosus Melastomataceae Montane cloud forest and lowland forest Hoorn 1993 Ilexpollenites sp. Aquifoliaceae, Ilex Montane cloud forest and lowland forest Thiergart 1937 ex Potonie 1960 Jandufouria saemrogiformis Bombacaceae, Catostemma Lowland forest, along creeks and rivers Germeraad et al. 1968 Kuylisporites waterbolkii Cyatheaceae, Cyathea horrida Montane region Potonie 1956 Laevigatosporites catanajensis Blechnaceae, Blechnum Lowland to high mountains, swamps and marshes Germeraad et al. 1968 Magnaperiporites spinosus Gonzalez-Guzman 1967 Magnastriatites grandiosus Pteridaceae, Ceratopteris Aquatic ferns, shallow lakes and rivers (Kedves & Sole de Porta 1963) Dueñas 1980 Margocolporites vanwijhei Leguminosae, Caesalpiniodeae, Caesalpinea Coastal vegetation Germeraad et al. 1968 bonduc or coriaria Matonisporites mulleri Matoniaceae-Dicksoniaceae-Cyatheacea, Playford 1982 Hemitelia Mauritidiites franciscoi Palmae, Mauritia Lowland swamps (Van der Hammen 1956) Van Hoeken- Klinkenberg 1964 Monoporopollenites annulatus Poaceae Open vegetation and fl oating meadows (Van der Hammen, 1954) Jaramillo & Dilcher 2001 Multimarginites Acanthaceae, Trichantera-Bravaisia Lowland forest Germeraad et al. 1968 vanderhammenii Psilastephanocolporites Sapotaceae Lowland forest Hoorn 1994a marinamensis Psilastephanocolporites Hoorn 1994a matapiorum Psilastephanocolporites Rhizophoraceae? Coastal mangrove vegetation Hoorn 1993 schneideri Perfotricolpites digitatus Convolvulaceae, Merremia Lowland forest Gonzalez-Guzman 1967 Perinomonoletes spp. Aspleniaceae, Asplenium-Thelypteraceae Krutzsch 1967 (Thelypteris) Perisyncolporites pokornyi Malpighiaceae Lowland forest Germeraad et al. 1968 Podocarpidites sp. Podocarpaceae, Podocarpus Montane and lowland forest Cookson 1947 ex Couper 1953 Polyadopollenites spp. Leguminosae, Mimosoideae Lowland forest Pfl ug & Thomson 1953 Polyadopollenites mariae Leguminosae, Mimosoideae, Acacia Lowland forest Dueñas 1980 Polypodiaceoisporites potoniei Pteridaceae, Pteris Lowland to high mountains Kedves 1961 Proteacidites cf. triangulatus Sapindaceae-Proteaeceae Lorente 1986 Proxapertites tertiaria Annonaceae, Crematosperma Lowland forest Van der Hammen & Garcia Mutis 1965 110/24/2009 1:57:02 Shobha

0 (Continued) / 2 4 / 2 0 0 9

1 : 5 7 : 0 2

S h o b h a HHoorn_ch19_Final.indd 324 o o r n _ c h 1 9 _ F i n a l . i n Table 19.3 Continued. d d

3 2

4 Pollen/spores Amazonia Taxonomic affi nity Ecology Author* (Neogene)

Psiladiporites minimus Moraceae, Ficus-Artocarpus-Sorocea Lowland forest Van der Hammen & Wijmstra 1964 Psiladiporites redundantis Moraceae Lowland forest Gonzalez-Guzman 1967 Psilamonocolpites amazonicus Palmae, Euterpe Poorly drained soils, lowland forest Hoorn 1993 Psilamonocolpites nanus Palmae Lowland forest Hoorn 1993 Psilamonocolpites rinconii Palmae Lowland forest Dueñas 1986 Psilaperiporites minimus Amaranthaceae-Chenopodiaceae Regali et al. 1974 Psilaperiporites multiporus Hoorn 1994b Psilastephanocolporites fi ssilis Polygalaceae Leidelmeyer 1966 Psilastephanoporites herngreenii Apocynaceae Lowland forest Hoorn 1993 Psilatricolpites acerbus Gonzalez-Guzman 1967 Psilatricolpites anconis Hoorn 1994a Psilatricolpites minutus Gonzalez-Guzman 1967 Psilatricolpites papilioniformis Regali et al. 1974 Psilatricolpites pulcher Wijmstra 1971 Ladakhipollenites simplex (Gonzalez-Guzman, 1967) Jaramillo & Dilcher 2001 Psilatricolporites aff. Sapotaceae Sapotaceae Lowland forest Van der Hammen 1956 ex Van der Hammen & Wijmstra 1964 Psilatricolporites atalayensis Hoorn 1993 Psilatricolporites costatus Dueñas 1980 Psilatricolporites crassoexinatus Hoorn 1993 Lanagiopollis crassa Theaeceae, Pelliciera rhizophora Coastal mangrove vegetation, behind Rhizophora (Van der Hammen & Wymstra 1964) Frederiksen, 1988 Psilatricolporites cyamus Van der Hammen & Wijmstra 1964 Psilatricolporites devriesii Humiriaceae, Humiria Lowland forest Lorente 1986 Psilatricolporites divisus Sapotaceae Lowland forest Regali et al. 1974 Psilatricolporites exiguus Hoorn 1993 Psilatricolporites garzonii Hoorn 1993 Psilatricolporites labiatus Sapotaceae, Pouteria Rainforest, along creeks and rivers Hoorn 1993 Psilatricolporites magniporatus Leguminosae? Hoorn 1993 Psilatricolporites normalis Gonzalez-Guzman 1967 Psilatricolporites obesus Sapotaceae Lowland forest Hoorn 1993 Ranunculacidites operculatus Euphorbiaceae, Alchornea Lowland and montane forest, in Amazonia (Van der Hammen & Wymstra, 1964) along rivers Jaramillo & Dilcher 2001 110/24/2009 1:57:03 Shobha 0 / 2

4 Psilatricolporites silvaticus Burseraceae-Sapotaceae Lowland forest Hoorn 1993 / 2 0 0 9

1 : 5 7 : 0 3

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3 2 5 Tetracolporopollenites Sapotaceae Lowland forest (Dueñas 1980) Jaramillo & Dilcher 2001 transversalis Psilabrevitricolporites triangularis (Van der Hammen & Wymstra 1964) Jaramillo & Dilcher 2001 Psilatricolporites varius Dueñas 1983 Psilatricolporites venezuelanus Lorente 1986 Psilatriletes aff. Lophosoria Psilatriletes aff. Pytirogramma Psilatriletes lobatus Hoorn 1994b Psilatriletes peruanus Pteridaceae, Pteris rangiferina Lowland to high mountains Hoorn 1994b Psilatriporites corstanjei Rubiaceae, Faramea? Montane and lowland forest Hoorn 1993 Psilatriporites desilvae Leguminosae, Caesalpinioideae Lowland forest Hoorn 1993 Psilatriporites sarmientoi Hoorn 1993 Retibrevitricolpites retibolus Leidelmeyer 1966 Retibrevitricolpites yavarensis Hoorn 1993 Retimonocolpites absyae Myristicaceae, Virola Marsh and lowland rain forest Hoorn 1993 Retimonocolpites longicolpatus Palmae Lowland forest Lorente 1986 Retimonocolpites maximus Palmae Lowland forest Hoorn 1993 Retimonocolpites retifossulatus Palmae Lowland forest Lorente 1986 Retistephanoporites Bombacaceae, Quararibaea Marsh and lowland rainforest Lorente 1986 crassiannulatus Retitricolpites lewisii Wijmstra 1971 Retitricolpites antonii Gonzalez-Guzman 1967 Retitricolpites caquetanus Bombacaceae-Tiliaceae? Lowland forest Hoorn 1994a Retitricolpites colpiconstrictus Hoorn 1994a Retitricolpites depressus Wijmstra 1971 Retitricolpites lalongatus Wijmstra 1971 Retitricolpites lorenteae Bombacaceae, Bombax Lowland forest, along creeks and rivers Hoorn 1993a Retitricolpites maledictus Gonzalez-Guzman 1967 Retitricolpites maturus Gonzalez-Guzman 1967 Retitricolpites simplex Anacardiaceae? Lowland forest Gonzalez-Guzman 1967 Retitricolpites tuberosus Bombaceae-Tiliaceae? Lowland forest Hoorn 1994a Retitricolpites wijningae Sterculiaceae-Tiliaceae? Hoorn 1994a Retitricolporites caputoi Hoorn 1993 Retitricolporites crassicostatus Rubiaceae Montane and lowland forest Van der Hammen & Wijmstra 1964

110/24/2009 1:57:04 Shobha Retitricolporites crassopolaris Hoorn 1994a 0 / 2

4 Retitricolporites ellipticus Van Hoeken-Klinkenberg 1964 / 2 0 0 9

(Continued)

1 : 5 7 : 0 4

S h o b h a HHoorn_ch19_Final.indd 326 o o r n _ c h 1 9 _ F i n a l . i n Table 19.3 Continued. d d

3 2

6 Pollen/spores Amazonia Taxonomic affi nity Ecology Author* (Neogene)

Rhoipites guianensis Tiliaceae-Sterculiaceae (Van der Hammen & Wymstra 1964) Jaramillo & Dilcher 2001 Rhoipites hispidus (Van der Hammen & Wymstra 1964) Jaramillo & Dilcher 2001 Retitrescolpites? irregularis Euphorbiaceae, Amanoa Lowland forest, along creeks and rivers (Van der Hammen & Wymstra 1964) Jaramillo & Dilcher 2001 Retitricolporites kaarsii Euphorbiaceae, Dalechampia Lowland forest Hoorn 1993 Retitricolporites latus Wijmstra 1971 Retitricolporites leticianus Hoorn 1993 Retitricolporites milnei Hoorn 1993 Retitricolporites oblatus Hoorn 1994a Retitricolporites poriconspectus Leguminosae Hoorn 1994a Retitricolporites pygmaeus Hoorn 1994a Retitricolporites santaisabelensis Hoorn 1994a Retitricolporites solimoensis Hoorn 1993 Retitricolporites ticuneorum Hoorn 1993 Retitricolporites wijmstrae Hoorn 1994a Retitriporites aff. Duroia Rubiaceae Montane and lowland forest (Van der Hammen 1956) Ramanujam 1966 Retitriporites dubiosus Gonzalez-Guzman 1967 Retistephanoporites angelicus Gonzalez-Guzman 1967 Rugotriletes sp. Van der Hammen 1956 ex Potonie 1956 Rugutricolporites spp. Gonzalez-Guzman 1967 Rugutricolporites arcus Chrysobalanaceae, Licania Lowland forest and savannas Hoorn 1993 Syncolporites anibalii Sapindaceae Lowland forest Hoorn 1994a Stephanocolpites sp. Passifl oraceae? Van der Hammen 1954 ex Potonie 1960 Stephanocolpites evansii Muller et al. 1987 Syncolporites spp. Van der Hammen 1954 ex Potonie 1960 Syncolporites incomptus Loranthaceae? Van Hoeken-Klinkenberg 1964 Spirosyncolpites spiralis Gonzalez-Guzman 1967 Scabratriporites redundans Gonzalez-Guzman 1967 Striatopollis catatumbus Leguminosae, Caesalpinoideae Lowland forest (Gonzalez-Guzman 1967) Takahashi and Jux 1989 Syncolporites poricostatus Myrthaceae Montane and lowland forest Van Hoeken-Klinkenberg 1966 110/24/2009 1:57:05 Shobha 0 / 2 4 / 2 0 0 9

1 : 5 7 : 0 5

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3 2 7 Trichotomosulcites Palmae, Bactris Lowland forest Couper 1953 Verrucatosporites spp. Pfl ug 1952 ex Potonie 1956 Verrucatosporites usmensis Polypodiaceae, Stenochlaena palustris Terrestrial, montane and lowland forest (Van der Hammen 1956) Germeraad et al. 1968 Verrucatotriletes cf. bullatus Cyatheaceae, Alsophyla Montane region Van Hoeken-Klinkenberg 1964 Verrutricolporites rotundiporis Van der Hammen & Wijmstra 1964 Verrutriletes spp. Van der Hammen 1956 ex Potonie 1956 Zonocostites duquei Rhizophoraceae, Rhizophora Coastal mangrove vegetation Germeraad et al. 1968

Zonocostites ramonae Rhizophoraceae, Rhizophora Coastal mangrove vegetation Dueñas 1980

Algae Botryococcus Chlorophyta, Botryococcus Planktonic algae, fresh water Pediastrum Chlorophyta, Botryococcus Planktonic algae, fresh water

Marine organisms Dinofl agellate cysts Dinofl agellate cysts Fresh and marine waters Foraminifer linings

Reworked Gemmamonocolpites (Eocene) Gemmastephanoporites (Paleogene) Elaterate pollen (Cretaceous) Acritarch (Paleozoic) Spores (Paleozoic) Retitricolpites type 920 (Venezuela)

*Author references are given in Jaramillo & Rueda (2008). 110/24/2009 1:57:05 Shobha 0 / 2 4 / 2 0 0 9

1 : 5 7 : 0 5

S h o b h a 328 C. Jaramillo et al.

The most characteristic palynological associations in the fl uvial Late Pliocene-Pleistocene settings contained a wide variety of rainforest taxa belonging to families such as the Arecaceae, Melastomataceae, Sapotaceae, There is a large hiatus in sedimentation in Amazonia during the Euphorbiaceae, Leguminosae, Annonaceae and Malpighiaceae Pliocene to Early Pleistocene (Latrubesse et al. 2007). Subsidence amongst many others (see Plate 13 & Table 19.3). The most abun- in the western Amazonian basins ceased and deposition became dant taxa were those nearest to the aquatic depositional environ- confi ned to the increasingly incised valleys of the major rivers ment such as Mauritia (Mauritiidites), a palm that formed palm in the region and the Amazon Fan (see Chapter 11). Potential swamps, accompanied by taxa from the fl uvial overbanks such as outcrops and borehole intervals containing Late Pliocene and Amanoa (Retitrescolpites? irregularis), Alchornea (Ranunculacidites Pleistocene strata may be found in the sub-Andean zone. operculatus) and Malvaceae (several types). The aquatic (mostly freshwater) nature of these settings is confi rmed by taxa such as The Neogene of northern South America: the Urumaco region the fern Ceratopteris (Magnastriatites grandiosus), a small aquatic fern bordering lakes and riverbanks (Germeraad et al. 1968) and The Urumaco Formation is formed by Upper Miocene deltaic the algae Botryococcus and Azolla. This predominantly fl uvial deposits that were accumulated in the Falcon Basin, western setting was occasionally disrupted by marine infl uence, as con- Venezuela. Lithologically, the formation is characterized by a fi rmed by the presence of a brackish-water association formed by complex alternation of medium- to fi ne-grained sandstone, the mangrove pollen of Rhizophora (Zonocostites ramonae) and organic-rich mudstone, coal, shale and thick-bedded limestone marine palynomorphs such as dinofl agellate cysts and chitinous coquinas. These sediments were deposited in a prograding strand- foraminiferal test linings. plain-deltaic complex. The thickness of the Formation ranges between 1100 and 1800 m (Díaz de Gamero & Linares 1989). Middle to early Late Miocene Based on lithofacies, the formation is divided into three units. Shales of the Lower and Upper members represent deposition This time period is characterized by smectite-rich Andean- of low-energy suspension on the shelf and prodelta. Hummocky derived sediments and wetland expansion into western Central cross-bedded sandstones represent progradation of wave- and Amazonia. The pre-existing rainforest was fragmented and storm-dominated deposition in the delta front, locally overlain extensive wetlands developed. Palynologically, this period is by massive mudstones and organic-rich fi ne-grained sediments characterized by an increment in the diversity of fern spores, of the interdistributary bay in the Lower member. Channelized increase of grasses (Monoporopollenites annulatus) and a pre- sandstones in the Middle member represent deposition in termi- dominance of palms such as Mauritia, Grimsdalea magnaclavata nal distributary channels. Subaquatic dunes formed the sandy fi ll an extinct taxon, Euterpe and Korthalsia. The palynological assem- of these highly incised channels. The Upper member was depos- blage also includes taxa indicative of an Andean source such as ited mainly on the delta plain. Podocarpus, Hedyosmum, Cyatheaceae, Hemitelia and Alsophyla. Palynofl oras from the Urumaco Formation are similar to Episodic marine intervals are characterized by Rhizophora Miocene fl oras from Amazonia (Table 19.4). The high degree of (Zonocostites ramonae) and marine palynomorphs (see Plate 13 & similarity suggests a continuation of the Amazonian forest into the Table 19.3). There are several intervals with fl uvial environments Urumaco region of northwestern Venezuela during the Miocene. with tidal infl uence prevailing, although the aquatic environment The latest Miocene-Early Pliocene Codore Formation over- was predominantly freshwater. The latter environments were lies the Urumaco Formation. It is composed of grey-mottled to dominated by grasses (Monoporopollenites annulatus), Asteraceae reddish massive-bedded mudstones interbedded with thick- to (Echitricolporites spinosus) and ferns (Hoorn 1993, 1994b). thin-bedded, massive, fi ne-grained sandstones, and fi ning-upward sequences of thick- to medium-bedded trough cross-stratifi ed, Late Miocene-Early Pliocene medium- to coarse-grained sandstone. The Codore Formation accumulated in a fl oodplain environment, exposed during long The fi nal part of the Neogene Amazonian sedimentary record periods to subaerial conditions, refl ecting a fl uctuating water is represented in the Late Miocene to Early Pliocene sediments table. The contact between the Urumaco and Codore Formations in the Acre and Amazonas states (Brazil). Palynological data represents a major change in the dynamics of the sedimentary suggest a diverse and well-structured forest with pollen types environments. This change is probably related to the collapse of the belonging to species from all forest strata, including grasses, gigantic Urumaco Delta during the Late Miocene and its replace- herbs (Gomphrena), understorey (Rauvolfi a) and canopy species ment with red-bed deposits that show a decrease in subsidence, (Geissospermum, Sapium) as well as diverse types of climbing sediment supply, subaerial exposure and palaeosoil formation, ferns (Lygodium) and epiphytes (Polypodium) (see Plate 13 & |and possibly correlates with a major uplift of the northern Andes Table 19.3). The Amazon river landscape was well established and the eastward shift in the course of a proto-Orinoco River (Diaz by this time – the environmental stability allowed extensive de Gamero 1996; Quiroz & Jaramillo in press). A large change has development of the Amazon terra fi rme forest. Approximately also been documented in the fi sh faunas (see Chapter 17). Floras 30 plant families have been identifi ed in this time period, with of the Codore Formation do not resemble Miocene Amazonian a predominance of Arecaceae, Poaceae, Malvaceae, Euphorbia- palynofl oras, indicating that the Amazon-type of forest in the ceae (Alchornea), Malpighiaceae, Humiriaceae (Humiria) and Urumaco region was replaced by the dry vegetation that domi- Melastomataceae (Miconia). nates the region today. This change could also be correlated with

HHoorn_ch19_Final.inddoorn_ch19_Final.indd 332828 110/24/20090/24/2009 1:57:061:57:06 ShobhaShobha Table 19.4 Pollen and sporomorph taxa shared between the Upper Miocene Urumaco Formation of Venezuela and Miocene deposits of western Amazonia.

Bombacacidites araracuarensis Polyadopollenites mariae B. baculatus Proteacidites triangulatus B. brevis Psilabrevitricolporites triangularis B. muinaneorum Psilamonocolpites medius B. nacimientoensis P. nanus B. psilatus P. operculatus Burseraceae undifferentiated P. rinconii Catostemma type Psilaperiporites minimus Chenopodipollis spp. P. multiporatus Clavainaperturites microclavatus P. robustus Crassiectoapertites columbianus Psilastephanocolporites matapiorum Crassoretitriletes vanraadshooveni Psilatricolporites caribbiensis Cyatheacidites annulatus P. costatus Cyclusphaera scabrata P. devriesii Deltoidospora adriennis P. divisus Echidiporites barbeitoensis P. labiatus Echiperiporites akanthos P. magniporatus E. estelae P. pachydermatus Echitricolporites maristellae P. silvaticus E. spinosus P. vanus Echitriletes muelleri P. venezuelanus Fenestrites longispinosus Retitricolpites colpiconstrictus F. spinosus R. simplex Foveotriletes ornatus R. amazonensis Grimsdalea magnaclavata R. caputoi Heterocolpites incomptus R. fi nitus Jandufouria seamrogiformis R. kaarsii Kuylisporites waterbolkii R. marianis Laevigatosporites catanejensis R. oblatus Lanagiopollis crassa R. poriconspectus Magnastriatites grandiosus R. santaisabelensis Malvacipollis spp. R. ticuneorum Margocolporites vanwijhei Retitriletes sommeri Mauritiidites franciscoi franciscoi Retitriporites dubiosus M. franciscoi minutus Rhoipites guianensis Melastomataceae type R. hispidus Monoporopollenites annulatus R. squarrosus Multimarginites vanderhammenii Rugutricolporites arcus Pachydermites diederixi Tetracolporopollenites maculosus Perfotricolpites digitatus T. transversalis Perisyncolporites pokornyi Zonocostites ramonae

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the extensive development of the tropical savannas in the latest vegetation and climate, and it has been studied from Quaternary Miocene, which shrunk the rainforest to its modern extent. deposits of the Amazon Fan (Piperno 1997). It may be pos- sible to recover phytoliths from older Amazonian rocks if new techniques are applied, as has been done in Eocene rocks from Palaeobotany North America (Strömberg 2004).

Plant fossils as a potential tool to reconstruct the Amazon rainforest Evidence of pre-Miocene rainforests in South America

Macrofossil plant remains, mostly leaves, woods and seeds, have The fossil record of South American fl oras has been compiled been widely reported throughout the Amazon drainage basin previously (Romero 1993; Burnham & Graham 1999; Burnham from Miocene to Quaternary deposits (Hoorn 1994b, 2006; & Johnson 2004). All evidence collected from macro and micro Rossetti & Goes 2004; Campbell et al. 2006; Antoine et al. 2006, fossils suggests that during the Eocene, Neotropical rainfor- Goillot et al. 2007; Latrubesse et al. 2007; Pons & De Franceschi ests became established in terms of physiognomy, diversity and 2007; Olivier et al. 2008). However, only a few plant localities have fl oristic composition. Pre-Eocene evidence for rainforests in been extensively collected and studied (Rossetti & Goes 2004; South America is scant; however, recent work in Colombia has Pons & De Franceschi 2007). Here we briefl y highlight several revealed that these biomes have been present at least since the palaeobotanical methods that should be kept in mind for future Late Cretaceous. A Maastrichtian assemblage known as Guaduas studies from Amazonia. fl ora from the central Andes of Colombia, located today at about Leaves are among the most abundant fossil remains in fl uvial 2700 m above sea level, has shown that a rainforest was already and lacustrine environments (Burnham et al. 1992), and dicot established (Gutierrez & Jaramillo 2007). This fl ora is still being fossil leaves could be used to reconstruct the palaeoclimate. Leaf studied, but preliminary analyses show that leaf physiognomy was margin and area analyses (Wolfe 1979; Wilf 1997; Wilf et al. 1998) dominated by mesophyll-macrophyll leaf sizes with brochido- can, respectively, be used to reconstruct past mean annual tem- dromous-eucamptodromous venation and entire margins, there- peratures and precipitation. These methods are based on modern fore suggesting a warm and wet palaeoclimate, as is seen in today’s correlations that relate margin and area of dicot leaves to climatic tropical rainforest. However, the Guaduas fl ora lacks key fl ori- parameters. A new method, which relates the area of the fossil stic elements that are present in modern Neotropical fl oras leaves to the extant scaling relationship between petiole width (e.g. legumes). squared and leaf mass (Royer et al. 2007), could also be used to A second assemblage from Colombia is the Cerrejón fl ora reconstruct quantitatively the mean annual precipitation for the (Wing et al. 2004), found in outcrops from Guajira Peninsula and Amazon forest in the past. excavated in the open-pit Cerrejón coal mine. This fl ora is Middle- The macrofossil plant record also could give us clues about the Late Paleocene in age, and it was deposited in ancient lagoonal origin and age of the high plant diversity of Amazonia, which is and fl ooded coastal plains environments (Jaramillo et al. 2007a). perhaps one of the most discussed topics in angiosperm evolu- The palaeoclimate has been reconstructed from leaf margin and tion. For instance, fossil fl owers, seeds, fruits, leaves and wood can area analysis, giving a mean annual palaeotemperature in excess be used to assess plant diversity in the geological past (Wing et al. of 29°C and an annual precipitation greater than 4 m (Herrera 1995; Wilf & Johnson 2004). Insect damage traces in leaves can et al. 2008b). Floristically, the fl ora is indistinguishable from liv- also give information about consumers (Wilf et al. 2000), correla- ing Neotropical fl oras and is dominated by Fabaceae, Arecaceae, tions between feeding diversity and climate changes, extinctions Malvaceae, Lauraceae, Araceae, Zingiberales, Menispermaceae, and plant diversity (Labandeira et al. 2002). Euphorbiaceae, Annonaceae, Anacardiaceae, Meliaceae and Fossil woods may be frequently identifi ed at family level based Flacourtiaceae (Doria et al. 2008; Herrera et al. 2008a, 2008b). on anatomical characters, offering a good opportunity to record These two macrofl oras from Colombia are remarkable evi- plant families in the Amazon Basin. As indicators of climate, dence of ancient tropical biomes, both showing that rainforest tropical fossil woods do not show a strong correlation between leaf physiognomy was established during the early stages of the temperature and the growth of tree rings (e.g. Chowdhury 1964). rainforests in northern South America. Both fl oras also have low However, recent techniques using anatomical characters such as plant diversity (Gutierrez & Jaramillo 2007; Jaramillo et al. 2007a; percentages of spiral thickenings present in vessels with a diam- Herrera et al. 2008b). eter less than 100 µm, and ring-porous vessels on dicot woods are well correlated with mean annual temperature (Wiemann et al. 1998). Otherwise, chemical characteristics of fossil woods may be Macrofossil plant records from the Miocene of the correlated with palaeoclimate proxies (Poole & van Bergen 2006). Amazonia When fossil woods are found in situ and the base of the trunk is preserved, it is possible to calculate the structure of the forest The records of plant macrofossils from Miocene Amazonian based on the relationship between basal trunk diameter and tree deposits are relatively sparse. This is due to vegetation cover of height (Rich et al. 1986; Lehman & Wheeler 2001). possible outcrops. Furthermore, little attention has been paid in Phytoliths are microscopic silica fl akes present in the vascular the past to wood and leaf remains, which are commonly men- system of only certain plant families, mostly monocots (Piperno tioned in stratigraphic studies of Miocene and younger rocks 1988). The phytolith record offers a window to past changes of (Hoorn 1994b, 2006; Rossetti & Goes 2004; Campbell et al. 2006;

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Antoine et al. 2006; Pons & De Franceschi 2007; Goillot et al. a specifi c sample size. This is termed rarefaction analysis, a tech- 2007; Latrubesse et al. 2007; Olivier et al. 2008). nique that calculates the number of species expected for a given A total of 24 angiosperm families have been reported from sample size smaller than the actual sample (Sanders 1968). This Miocene rocks of Amazonia. Duarte (2004) described 17 fami- technique is used to account for differences in diversity result- lies corresponding to 19 genera from fossil leaves of the Miocene ing from different sample sizes. All analyses were done in R for Pirabas Formation from Brazil. This formation seems to have Statistical Computing (R-Development-Core-Team 2005) and the been deposited in a littoral environment. Among the families R package Vegan (Oksanen et al. 2005). reported are Nyctaginaceae, Lauraceae, Dilleniaceae, Theaceae, We compared the rarefi ed palynological diversity at a counting Caryocaraceae, Chrysobalanaceae, Euphorbiaceae, Rutaceae, level of 208 grains (the pollen number of the smallest sample in Meliaceae, Sapindaceae, Malvaceae, Myrtaceae, Melastomataceae, the set) for samples from several Amazonian sites. Palynological Rhizophoraceae, Ebenaceae, Rubiaceae and Rapataceae. The aver- data for the Miocene were taken from the literature (Hoorn 1993, age size of these fossil leaves is mesophyll, abundant acuminate 1994a, 1994b, 2006), and several cores from the Quaternary apexes are preserved, and most leaves have entire margins suggest- were also used, including Piusbi (Behling et al. 1998), dos Patas ing a warm and humid climate. However, a more specifi c analysis (Colinvaux et al. 1996), Curucab (Behling 1996) and Monica of the leaf characters has not yet been carried out. Floristically, the (Berrio 2002). All sites were attributed to one of four time inter- Pirabas fl ora contains some of the most important families that vals and the average diversity at a counting level of 208 grains was make up modern Neotropical lowland rainforests (e.g. Lauraceae, calculated for each site. Euphorbiaceae, Meliacaeae and Malvaceae). Fossil leaves related to Malvaceae (Bombacacidites) have also been reported from 1 Lower Miocene: Mariñame, Tres Islas, Santa Isabel, core mangrove deposits of the Miocene Barreiras Formation of Brazil AS04a-AM (181.8 to 275 m); (Dutra et al. 2001). 2 Middle Miocene: Pebas, Iquitos, core AS04a-AM (89 to Fossil woods from the Middle Miocene Pebas Formation of 181.7 m); Peruvian Amazonia have been assigned to the Anacardiaceae 3 Upper Miocene: Mocagua, Los Chorros East and West, Santa (Anacardium), Clusiaceae (Calophyllum), Combretaceae (Buche- Sofi a, and Apaporis, core AS04a-AM (23.5 to 88.9 m). navia and Terminalia), Fabaceae (Andira/Hymenolobium), Humi- 4 Quaternary: Piusbi, Curucab, Monica and Dos Patas. riaceae (Humiriastrum), Lecythidaceae (Cariniana and Eschweilera) and Meliaceae (Guarea) (Pons & De Franceschi 2007). The lack There exists a slight trend toward decreasing diversity from the of growth rings and the family composition suggest that these Neogene to the Quaternary (Fig. 19.3). However, the pattern is fossil woods were part of terra fi rme lowland tropical rainforests neither clear nor signifi cant. The outcomes may have been infl u- (Pons & De Franceschi 2007). However, additional anato mical enced by the fact that the Neogene pollen data were collected with characters should be taken into account besides the family com- other goals in mind (mainly biostratigraphy and palaeoecology), position to distinguish between riparian and terra fi rme habitat. other than analysing diversity over time. Furthermore, different Fossil leaves and woods suggest that fl oristically the Miocene depositional environments may have been analysed. Given the rainforests were similar to modern Neotropical lowland rain- cooling trend of the Neogene together with the areal reduction of forests, even at the generic level. The study of macrofossils from the fl ooded forest, which is a major provider of pollen and spores Neogene Amazonia is a promising fi eld, and might yield a better for the fossil record, a reduction in diversity is to be expected. understanding of the palaeoclimate, the evolution of angiosperm However, further studies are needed to test this hypothesis. families and animal–plant interactions, and the structure of the Miocene rainforests. Quaternary

Diversity analysis

Late Miocene In this chapter, the word ‘diversity’ is used in its original sense to denote the number of species (Rosenzweig 1995), which is also called ‘richness’. Pollen can be a useful tool for estimating plant

diversity through time (e.g. Morley 2000). It mostly refl ects Middle Miocene genera and families (Germeraad et al. 1968; Jackson & Williams 2004), indicating that it can be used to track plant diversity at that taxonomic level through geological time. We assessed Amazonian Neogene within-sample diversity Early Miocene (the number of species in a given sample) using a technique #species 10 20 30 40 50 60 called rarefaction (Sanders 1968; Hurlbert 1971). Estimating the number of species in a sample involves counting the species Rarefied diversity, cutoff 208 in a given sample. However, the number of species depends on Fig. 19.3 Rarefi ed diversity at a counting level of 208 grains the number of pollen grains counted; thus, as more grains are for the Miocene and Quaternary of the Amazonian Basin. counted, more species are found. In order to compare the diver- Each point represents the average diversity of a site. The bar sity among different samples, data must fi rst be standardized to represents the 95% confi dence interval.

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Conclusions in Amazonia, and the birth of the modern Amazon River system. Palaeogeogr Palaeocl 239, 166–219. The Amazonian rainforest has had a long and dynamic history. Chowdhury, K.A. (1964) Growth rings in tropical trees and taxonomy. Middle Cretaceous Amazonian fl oras were dominated by non- J Indian Bot Soc 43, 334–343. Colinvaux, P.A., Oliveira, P.E.D., Moreno, J.E., Miller, M.C., Bush, angiosperm taxa, whereas by the Paleocene, rainforests were M.B. (1996) A long pollen record from lowland Amazonia: forest dominated by angiosperms and were already populated by the and cooling in glacial times. Science 274, 85–88. plant families that are dominant in modern tropical Amazonian Daemon, R.F. (1975) Contribuição à datação da Formação Alter do rainforests. The Neogene uplift of the Andes changed the drain- Chão, Bacia do Amazonas. Rev Bras Geoci 5, 78–84. age system from south-north to west-east, and from rivers being Daemon, R.F., Contreiras, C.J.A. 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