Pollen grains in quaternary sediments from the Campos Basin , state of Rio de Janeiro , Brazil : Core BU-91-GL-05

Here, we describe pollen grains extracted from a Pleistocene-Holocene sediment core (BU-91-GL-05; 22°48'45"S; 41°54'13"W) taken from the Albacora Slope (22°48'45"S; 41°54'13"W), located in the Campos Basin of the northern region of the state of Rio de Janeiro, Brazil. The analysis resulted in the identification and morphological description of 46 types of pollen: one of a gymnosperm genus (Podocarpus); and 45 of angiosperm taxa across 27 families-one family of monocotyledons (Poaceae) and 26 families (30 types) of dicotyledons. The most common angiosperm families were Amaranthaceae (Chenopodium, Amaranthus and Gomphrena); Fabaceae (Fabaceae type, Bauhinia, Inga and Canavalia); Malpighiaceae (Tetrapteris, Heteropteris and Peixotoa); Malvaceae (Sida, Abutilon, Hibiscus and Pseudobombax); Rubiaceae (Faramea, Borreria and Psychotria); Asteraceae (Eupatorium and tribe Vernonieae); Bignoniaceae (Bignoniaceae type, Adenocalymma and Tabebuia); and Onagraceae (Fuchsia and Ludwigia). The palynoflora in this study are associated with dense montane and submontane Atlantic Forest, semideciduous forest and restinga (coastal woodland), all of which are present in the state of Rio de Janeiro. Palynological analysis can provide important data about paleovegetation and paleoclimatic changes in the studied area during the Quaternary, specifically in the last 145,000 years.


Introduction
Morphological descriptions and taxonomic identification of quaternary pollen grains form marine sediments can allow inferences to be made about the paleovegetation, paleoclimate and paleoenvironment during the Upper Pleistocene-Holocene in coastal areas of southeastern Brazil.Fossil pollen grains and spores are morphologically similar to those produced by modern plants.Although the palynological records collected to date for southern and southeastern Brazil are relatively specific, these data constitute an important tool for the understanding of vegetation dynamics and paleoclimate, as well as for and paleoenvironmental reconstruction of the Pleistocene-Holocene (Behling et al. 2002;Freitas 2005;Luz et al. 2006;Medeanic et al. 2006;Freitas et al. 2007;Toledo et al. 2009).
Based on palynological analysis of sediment from the Campos Basin, located in the northern region of the state of Rio de Janeiro, Brazil, Behling et al. (2002) observed changes in paleovegetation with a predominance of grasses in glacial cycles and increases in arboreal and semideciduous forests during interglacial cycles.Undertaking Pleistocene-Holocene palynological analysis of the BU-91-GL-05 core, taken from the same basin, Freitas (2005) registered continental palynomorphs (cryptogamic spores, phanerogamic pollen grains, fresh water microalgae and microfungi).Vegetation types included taxa associated with Atlantic Forest (montane and lowland), semideciduous forest and restinga (coastal woodland), as well as herbs and hydrophytes.The percentage variations in the terrestrial palynomorphs indicated paleoenvironmental changes occurred during glacial and interglacial cycles over the past 145,000-150,000 years based on foraminiferal biozones.The morphological descriptions of spore and pollen types reveal a richness and diversity, in the same core, of pteridophyte and hydrophyte spores (Freitas et al. 2007) of periodically or totally flooded environments such as inundated brackish swamps, lagoon systems and flooded areas of pioneer formations of restinga, salt marshes and mangrove.
Palynological analyses coastal plain in northern part of the state of Rio de Janeiro indicate climatic oscillations from ca. 6,100 14 C yr BP to the present.Luz & Barth (2002) studied sediments from the nearby Lagoa de Cima, in the city of Campos dos Goytacazes, and registered spore-pollen indicators of Atlantic Forest, restinga, field vegetation, salt marshes and lagoon shores.The Holocene lacustrine sediment cores showed the expansion of the coastal plain with establishment of field vegetation between 6,500 and ca.4,000 14 C yr BP.These changes were probably mediated by relative sea level oscillations in the region during the Holocene (Luz et al. 2011).
In a paleoenvironmental reconstruction of the Lagoa Salgada, in the city of Macaé (state of Rio de Janeiro), Toledo et al. (2009) used multivariate statistical analyses in order to compare pollen records between surface and subsurface sediments.The authors determined that the recent vegetation became established in the region at ca. 2,500 14 C yr BP.
As can be se en in Fig. 1, the current vegetation formations in the northern region of the state of Rio de Janeiro include the following (Radambrasil 1983;IBGE 1992): Atlantic Forest; semideciduous forest; and pioneer formations with fluvial and marine influence (restinga, mangrove and salt marshes).
This work presents morphological descriptions of pollen grains recovered from quaternary marine sediments (Fig. 1).These data were associated with recent vegetation in the northern region of the state of Rio de Janeiro and constitute the first records of terrestrial palynomorphs on the slope portion of the Campos Basin in southeastern Brazil.

Study Area
The Campos Basin is located in the southeastern portion of the Brazilian continental margin in an area between the states of Espírito Santo (21°S, the Vitória ridge) and Rio de Janeiro (23°S, the Cabo Frio upwelling) (Fig. 1).The studied region has a warm climate with seasonal humidity in lowland regions, with rainy summers and dry winters.The average monthly rainfall ranges from 650 mm to 1000 mm, the dry season lasting 3-4 months (Nimer 1979).The average annual temperature in the largest city of the region (Campos dos Goytacazes) is 23°C.The coastal plain, including the Paraiba do Sul river delta, is extensive.It gradually decreases between positions 21°30'S and 22°15'S and receives fluvial and marine influence (Nimer 1979;Radambrasil 1983).
The recent vegetation in the northern state of Rio de Janeiro comprises plant formations associated with Atlantic Forest (lowland and montane), semideciduous forest, mangrove and restinga (Radambrasil 1983;IBGE 1992).Phytosociological data for northern Rio de Janeiro (Assumpção & Nascimento 2000;Costa & Dias 2001;Moreno et al. 2003;Pessoa & Oliveira 2006;Pimentel et al. 2007;Silva & Nascimento 2001) suggest that the region encompasses the so-called tabuleiro forests (coastal lowland forests on Tertiary deposits) in the lowlands and xeromorphic (restinga) vegetation in the coastal areas.
In the north of the state of Rio de Janeiro, there is a major protected area (Jurubatiba Coastal Woodlands National Park), managed by the Chico Mendes Institute for the Conservation of Biodiversity, encompassing multiple restinga ecosystems (Costa & Dias 2001;Pereira et al. 2004;Montezuma & Araujo 2007).

Material and methods
The marine core BU-91-GL-05 (22°08'12"S; 39°54'53"W) is 149.5 m long and was collected at a depth of 650 m, on the Albacora Slope, northern Campos Basin, located 150 km east of the city of Campos dos Goytacazes, in the northern part of the state of Rio de Janeiro (Fig. 1).The core sediments are composed mainly of organic muds.Sandy intercalations occur near the top of the core, at 63-65 m and 97-100 m.Slump or turbidite deposits also occur between 126.70-127.85m (Caddah et al. 1998) (Fig. 1).Using planktonic foraminiferal biostratigraphy, Vicalvi (1997;1999) calculated the estimated age of deposition of the sediments in the core in the last 145,000-150,000 years.Two sediment samples from the top of the core were submitted to 14 C-dating (Beta Analytic Inc., Miami, FL, USA).The ages derived were 13,210 ± 70 14 C yr BP for the 1.3-1.5 m interval and 20,020 ± 100 14 C yr BP for the 10.2-10.4m interval (Fig. 1; Tab. 1).Dates were calibrated using the IntCal09 curve (Ramsey et al. 2009) in the Calib 6.1.1 program (Stuiver & Reimer 1993).
For pollen analysis, we selected 43 samples of core BU-91-GL-05 (10-20 g each).Samples were treated using the standard techniques employed in palynofacies analysis (Tyson 1995;Mendonça Filho et al. 2002), which consist of removing the mineral fraction, with hydrochloric and hydrofluoric acids, and concentrating the resulting organic residue with a dense liquid (ZnCl 2 ; D=2.0 g/cm 3 ), in this case without oxidation.The samples were stored in the Laboratory of Plant Paleoecology at the National Museum of the Federal University of Rio de Janeiro.
We made standard morphological descriptions of pollen grains using characters such as polarity; symmetry; number, position and character of apertures; exine ornamentation; shape; and size (Punt et al. 2007) (Tab.2).These characteristics provide a sound basis for correlations between fossil and modern pollen grains, permitting their taxonomic classification.The identification of pollen grains was made on the basis of data obtained from the following bibliographic sources: Moreira et al. (2004), Souza et al. (2004), Carrijo et al. (2005), Gonçalves-Esteves et al. (2007), Mendonça et al. (2007a;2007b;2009;2010), Aguiar et al. (2008)), Peçanha et al. (2008), Loueuille et al. (2012) andMilward-Azevedo et al. (2010;2012).This was in addition to consulting the reference collection of the Álvaro Xavier Moreira Laboratory of Palynology in the Botany Department of the National Museum of the Federal University of Rio de Janeiro.The pollen type was characterized by establishing the proximity between the material analyzed and the taxonomic group (Salgado-Labouriau 1973;Lorscheitter 1989).The photomicrographs shown in Fig. 2 and Fig. 3 were obtained with a Zeiss light microscope in conjunction with the AxioVision software, version 6.0 (Carl Zeiss, Oberkochen, Germany).
Pollen descriptions (Tab.2) follow the classification system established in the Angiosperm Phylogeny Group III guidelines (Souza & Lorenzi 2008;, APG III 2009).The pollen types identified in core BU-91-GL-05 correspond to recent vegetation reported for Atlantic Forest (lowland and montane), semideciduous forest and restinga, as well as to the hygrophytes, herbs and other vegetation currently occurring in flooded coastal plain environments.These correlations were based on floristic and phytosociological surveys carried out on the northern of the Rio de Janeiro State (Tab.3).

Results and discussion
In the 43 samples taken from core BU-91-GL-05, we identified 46 pollen types (Fig. 2 and 3).These were distributed as follows (Tab. 2 and 3): one gymnosperm genus (Podocarpus); and 45 angiosperm types belonging to 27 families-15 types of a single family of monocotyledons (Poaceae) and 30 types across 26 families of dicotyledons.The families of angiosperms that were most representative in terms of the number of pollen types were Fabaceae, with four (Fabaceae type , Bauhinia, Inga and Canavalia), Amaranthaceae, with three (Chenopodium, Amaranthus and Gomphrena), Malpighiaceae, with three (Tetrapteris, Heteropteris and Peixotoa), Malvaceae, with three (Sida, Abutilon, Hibiscus and Pseudobombax), Rubiaceae, with three (Faramea, Borreria and Psychotria), Bignoniaceae, with three (Bignoniaceae type, Adenocalymma and Tabebuia), Asteraceae, with two (Eupatorium and tribe Vernonieae), and Onagraceae, with two (Fuchsia and Ludwigia).The wide spectrum of pollen types points to a dynamic paleovegetation environment throughout the Upper Pleistocene-Holocene in southeastern Brazil, especially in the north of the state of Rio de Janeiro.

Atlantic Forest
Arboreal taxa (Podocarpus and Ilex), as classified by the Brazilian Institute of Geography and Statistics (IBGE 1992) and Radambrasil (1983), are tree layer components derived from mixed and montane/upper montane Araucaria forest, at 400-2,000 m of elevation.Arboreal taxa of lowland tropical rain forest do occur, as represented by Euphorbiaceae (Alchornea and Croton), Myrtaceae and Rubiaceae, which occupy the slopes of coastal and inland mountains (Radambrasil 1983;IBGE 1992).According to Carauta & Rocha (1988), the Podocarpaceae arboreal family consists of high latitude woodlands along the length of the Paraíba do Sul River, in the state of Rio de Janeiro.Moreno et al. (2003) undertook a phytosociological survey in two areas of dense, submontane forest, at 50-250 m of elevation, in the foothills of the Imbé mountain range, near Campos dos Goytacazes, in the state of Rio de Janeiro (Fig. 1).The families Fabaceae, Myrtaceae, Euphorbiaceae and Rubiaceae were found to be quite species-rich in the area.The taxa most commonly found in the marine sediment examined in the present study (Tabebuia, Alchornea, Inga, Meliaceae, Trichilia, Myrtaceae, Psychotria and Symplocos) were also recorded for the Imbé region, on the coastal plain of the northern part of the state of Rio de Janeiro.Phytosociological studies of the shrub-arboreal component of a submontane forest in the Poço das Antas Biological Preserve (state of Rio de Janeiro) have shown that the most common botanical families are Euphorbiaceae, Fabaceae, Myrtaceae, Bignoniaceae, Sapindaceae, Boraginaceae, Meliaceae and Rubiaceae (Pessoa & Oliveira 2006).Our pollen data fit with the Garcinia, Inga, Myrtaceae, Alchornea, Asteraceae and Psychotria taxa.Some of the arboreal taxa recorded for the Atlantic Forest in the Paradise State Ecological Reserve, near the town of Cachoeira de Macacu, in the state of Rio de Janeiro (Tabebuia, Garcinia, Meliaceae, Myrtaceae and Psychotria) (Kurtz & Araujo 2000) were also seen in marine sediments of the Campos Basin.

Semideciduous forest
In floristic surveys of the Mata do Carvão forest, a remnant of the Mata Tabuleiros forest, located near Campos dos Goytacazes, Silva & Nascimento (2001) noted the species richness of the arboreal families Fabaceae, Euphorbiaceae, Bignoniaceae, Meliaceae, Myrtaceae, Sapindaceae and Rubiaceae.In sediment from the Albacora Slope, we found Tabebuia, Pseudobombax, Myrtaceae, Meliaceae, Polygala and Rubiaceae.Phytosociological data from the Pau Brasil Environmentally Protected Area, in the Emerenças Hills, near the city of Armação dos Búzios, which is in the lakes region of the state of Rio de Janeiro, indicate the dominance of Myrtaceae, Fabaceae and Euphorbiaceae (Kurtz et al. 2009).
Some of the taxa recorded in the present study (Tabebuia, Garcinia, Heteropteris, Pseudobombax, Meliaceae and Myrtaceae) belong to the shrub-arboreal component of semideciduous forests in coastal regions of the state of Rio de Janeiro.Bauhinia (Fabaceae) was also recorded by Kurtz et al. (2009) and is present in the lowland forest arboreal layer occupying the hills and coastal plains (Costa & Dias 2001).

Restinga
Considering the diversity of pollen types id entified and registered, as well as the proximity to the restingas in the study area, those pollen types have strong relationships with arboreal taxa of shrub and herbaceous vegetation, restinga and other pioneer formations.According to Rizzini (1997), restingas are found in regions with direct marine influence and consequently exhibit an enormous variety of vegetation types.Coastal area vegetation communities are directly affected by tidal fluctuations.The families (genera) commonly found near beaches and dunes include the following (IBGE 1992;Radambrasil 1983): Fabaceae (Canavalia), Poaceae (Paspalum), Apiaceae (Hydrocotyle), Erythroxylaceae (Erythroxylum), and Myrtaceae.
In a floristic analysis of restingas in the state of Rio de Janeiro, Pereira & Araujo (2000) showed that the most representative families are Fabaceae, Myrtaceae, Orchidaceae, Bromeliaceae, Rubiaceae, Cyperaceae, Asteraceae, Poaceae, Melastomataceae and Euphorbiaceae.The taxa identified in our study have also been reported in floristic and phytosociological studies of the restingas of Rio de Janeiro, especially along its northern coast.Among the plant communities in Jurubatiba Coastal Woodlands National Park, the following related herbaceous types have been recorded (Costa & Dias 2001): Amaranthaceae (Alternanthera, Blutaparon and Gomphrena); Apocynaceae; Ilex; Asteraceae (Eupatorium and Vernonia); Bignoniaceae (Adenocalymma, Arrabidaea and Tabebuia); Malvaceae (Pseudobombax, Abutilon and Hibiscus); Boraginaceae (Tournefortia); Clusiaceae (Garcinia); Ericaceae; Euphorbiaceae (Alchornea and Croton); Fabaceae (Bauhinia, Canavalia and Inga); Lentibulariaceae (Utricula-  The identity of the pollen grains from the one Poaceae family described in this paper was verified through assessment of their morphological features.However, it is not yet possible to distinguish all taxa down to the genus level.Coincidentally, a flora identified in restingas of the northern coast of Rio de Janeiro indicate that genera belonging to Poaceae occur in coastal environments, such as sandbanks (Andropogon, Eragrostis, Gymnopogon, Rhynchelytrum and Sporobolus); in flooded areas and in the transition between sandbanks and marshlands (Dac- In floristic studies of the areas surrounding the lagoons in the Grussaí-Iquipari drainage basin, near the municipality of São de João Barra, in northern Rio de Janeiro, Assumpção & Nascimento (2000) recorded four vegetation formations that also correspond to pollen types deposited in the Campos Basin during the Pleistocene-Holocene: beach grass/ marsh grass formation (Poaceae, Alternanthera, Blutaparon and Borreria); beach grass with shrubs (Myrtaceae, Poaceae, Desmodium, Polygala and Borreria); Clusia-dominated formations (Myrtaceae, Meliaceae, Tournefortia, Poaceae, Inga and Sapindaceae); and restinga (Bignoniaceae, Arrabidaea, Pseudobombax, Garcinia, Inga, Heteropteris, Myrtaceae and Sapindaceae).The pollen grains described are also related to the shrub-arboreal component in Coastal Woodlands National Park, near Lake Comprida and Lake Cabiúnas, along the northern coast of Rio de Janeiro.Pimentel et al. (2007) analyzed the taxa richness and diversity among beaches, dunes and Clusia-dominated formations.The taxa found were: Croton, Garcinia, Heteropteris, Ilex, Inga, Meliaceae, Tribe Vernonieae (Vernonia) and Myrtaceae.

Herbaceous vegetation
The Poaceae pollen grains identified in the present study are also related to restinga vegetation in open upper montane areas (Rizzini 1997) or grassy woodlands that occupy wetlands, near rivers and lakes and in association with Asteraceae and Cyperaceae (IBGE 1992).Taxa commonly associated with herbaceous vegetation include Poaceae, Amaranthus, Alternanthera, Gomphrena, Chenopodium, Borreria, Polygala, Utricularia, Asteraceae, Peixotoa, Desmodium, Ericaceae, Adenocalymma and Convolvulaceae.This association is characteristic of xerophytic and hygrophytic vegetation, reflecting grassland or open areas with some riparian or lacustrine influence.
The results of a palynological analysis carried out by Behling et al. (2002) in the Campos Basin suggest that grass-dominated ecosystems composed most of the landscape during glacial cycles in southeastern Brazil, thus reflecting a colder, drier climate in northern Rio de Janeiro.Palynological data from the Albacora Slope sediments, in the same basin, indicate the presence of grasses in the glacial and interglacial cycles (Freitas 2005).The low frequency of grasses in the samples analyzed (<10%) is more likely to be due to changes in sea level than to be a response to significant climatic changes in the northern region of the state of Rio de Janeiro during the Pleistocene-Holocene.

Flooded coastal plain environments
Coastal plain environments are home to a variety of habitats, including wetlands; fresh water lakes;, brackish and salt water lagoons; flood plains; and partially or periodically flooded forests (MMA 2002).Taxa observed in the present study-herbaceous (Poaceae, Polygonum, Ludwigia, Borreria, Polygala and Utricularia); shrub-arboreal (Vernonia, Stigmaphyllon, Garcinia, Alchornea, Croton, Inga, Desmodium, Pseudobombax, Meliaceae, Tabebuia and Ilex); and lianas (Passiflora, Sapindaceae, Psychotria)-also correspond to vegetation occurring in periodically or permanently flooded areas of the Jurubatiba Coastal Woodlands National Park.These exist in lakes, salt marshes and flooded coastal plains in the northern part of the state of Rio de Janeiro (Costa & Dias 2001;Bove et al. 2003).

Conclusions
On the basis of the morphological descriptions and taxonomic identification of pollen grains, we can make some inferences regarding the paleovegetation of continental areas adjacent to the Campos Basin during the Pleistocene-Holocene, thus contributing to the current body of research in the area.The pollen types identified in this study are attributed to the following, as currently found in the north of the state of Rio de Janeiro: dense lowland and montane rain forest; seasonal semideciduous forest, restinga; herbaceous vegetation; and hygrophytes common to wetland environments.

Figure 1 .
Figure 1.Map showing the location of core BU-91-GL-05, Albacora Slope, Campos Basin, state of Rio de Janeiro, Brazil, as well as the current distribution of vegetation in southeastern Brazil.