Late Aptian (Cretaceous) climate changes in

Palaeogeography, Palaeoclimatology, Palaeoecology 485 (2017) 543–560

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Late Aptian (Cretaceous) climate changes in northeastern Brazil: A reconstruction based on indicator species analysis (IndVal) Marcelo de Araujo Carvalho a,⁎, Cecília Cunha Lana b, Peter Bengtson c, Natália de Paula Sá a,d a

Laboratório de Paleoecologia Vegetal, Departamento de Geologia e Paleontologia, Museu Nacional, Universidade Federal do Rio de Janeiro, Brazil Gerência de Bioestratigrafia e Paleoecologia, CENPES, PETROBRAS, Rio de Janeiro, Brazil Institut für Geowissenschaften, Universität Heidelberg, Heidelberg, Germany d Programa de Pós-Graduação em Geologia, Departamento de Geologia, Universidade Federal do Rio de Janeiro, Brazil b c

a r t i c l e

i n f o

Article history: Received 26 December 2016 Received in revised form 6 July 2017 Accepted 9 July 2017 Available online 15 July 2017 Keywords: Palaeoenvironments Palynology Sea-level changes Sergipe Basin, Brazil

a b s t r a c t The flora preserved in upper Aptian rocks of South America and Africa is typical of warm climate conditions and commonly associated with semi-arid to arid climate. Warmth-loving conifers of the family Cheirolepidiaceae and their pollen Classopollis are recorded in upper Aptian rocks in most of the South Atlantic margin basins. However, an increase in indicators of humid conditions (e.g., ferns) is recorded in most sedimentary basins of Brazil. The method of indicator species analysis (IndVal) was applied as a tool for reconstructing the vegetation during the late Aptian. The IndVal index expresses which taxa are strongly associated with particular groups of samples. The vegetation reflects climate changes, and the IndVal indices illustrate how the taxa interacted through time and reveal patterns in the changing composition of the vegetation. The material studied derives from two well sections drilled through the Riachuelo Formation in the Sergipe Basin, GTP-17-SE (Angico Member, 70 samples) and GTP-24-SE (Taquari Member, 108 samples). The indicator species are strongly associated with particular stratigraphic intervals. IndVal indices for the Angico section indicate seven taxa associated with four intervals, viz. Classopollis classoides (Interval AS-1); Callialasporites segmentatus and Cicatricosisporites avnimelechi (Interval AS-2); Verrucosisporites spp. and Cicatricosisporites microstriatus (Interval AS-3); Araucariacites australis and Cyathidites spp. (Interval AS-4). Values for the Taquari section indicate nine taxa associated with four intervals, viz. Classopollis classoides (Interval TS-1); Uesuguipollenites callosus, Callialasporites segmentatus Bennettitaepollenites regaliae, Cyathidites spp., Cicatricosisporites spp. and Araucariacites australis (Interval TS-2); Retitriletes spp. (Interval TS-3); Araucariacites australis and Verrucosisporites spp. (Interval TS-4). Two phases, dry and wet, are recognized in both sections. The dry phase is characterized by high to very high abundance of Classopollis classoides. A conspicuous change in vegetation is recorded, with an increase in ferns and upland flora, in particular Araucariacites australis. A. australis is the second most abundant terrestrial palynomorph. In the late Aptian of South America and Africa Araucariacites is generally associated with an upland flora and warm and humid climates, which may explain its association with fern spores. The replacement of Classopollis by Araucariacites and ferns reflects a change from a dry to wet phase. The change in flora may be the result of dislocation of the Intertropical Convergence Zone (ITCZ) and a relative sea-level rise. © 2017 Elsevier B.V. All rights reserved.

1. Introduction The Cretaceous Period is generally conceived as one of the warmest periods in Earth history (e.g. Larson and Erba, 1999; Crowley and Zachos, 2000; Royer et al., 2007). However, the climatic effects on vegetation are poorly documented. The link between warm climate and plant distribution is here highlighted on the basis of palynological analyses. ⁎ Corresponding author at: Departamento de Geologia e Paleontologia, Museu Nacional, Universidade Federal do Rio de Janeiro, Quinta da Boa Vista s/n, CEP: 22040-040 São Cristóvão, Rio de Janeiro, Brazil. E-mail address: [email protected] (M.A. Carvalho).

http://dx.doi.org/10.1016/j.palaeo.2017.07.011 0031-0182/© 2017 Elsevier B.V. All rights reserved.

The late Aptian interval (113–123 Ma) was characterized by major global changes in climate, physiography, sea level, ocean circulation, and anoxic events (e.g., Cooper, 1977; Arthur and Schlanger, 1979; Bralower et al., 1993; Arai, 2014). A combination of these factors strongly affected life on land and in the oceans. At this time, fully marine conditions were being established in the South Atlantic Ocean (Koutsoukos et al., 1991), which created new habitats and affected sedimentary processes and climate on regional and global scales. Generally, the vegetation of northeastern Brazil during the Aptian is interpreted as adapted to semi-arid and arid climates (dry conditions). Warmth-loving conifers of the family Cheirolepidiaceae and their pollen Classopollis are often abundant in upper Aptian rocks in most of the continental margin basins of the South Atlantic. In several basins, the

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M.A. Carvalho et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 485 (2017) 543–560

Classopollis dominance coincides with evaporite deposits, as is also the case of the intracratonic Araripe Basin (Lima, 1976; Heimhofer and Hochuli, 2010). According to Dai et al. (2006), an important quantitative criterion in identifying communities is the presence and abundance of species in sampling units. However, not every species contributes equally to the identification of groups, and key indicator species are usually used for community classification. One of the greatest difficulties in ecology is to understand the vegetation dynamics (e.g., long life span of many plant groups, time lags in vegetation response to climate). For this purpose, several statistical indices, in particular ordination methods are used to observe patterns of interaction between taxa and the environment. Some of these indices are also applied to fossils with the same goal and in trying to understand the dynamics of palaeovegetation and palaeoenvironment characterization. One such index is the indicator species analysis (IndVal), with an incipient use in palaeontology (Caron and Jackson, 2007; Roucoux et al., 2013). Here, for the first time the IndVal proposed by Dufrêne and Legendre (1997) is applied as a method for reconstructing the vegetation during the late Aptian. The vegetation reflects changes in climate, and the IndVal of selected taxa illustrates how taxa interacted through time and reveals patterns in the changing composition of the vegetation. The numerical approach of IndVal reveals major changes in vegetation per interval unit obtained by ordination. The method produced evidence of vegetational changes that were not only climatically controlled but also ecologically modulated by local events, such as sea-level changes.

2. Geological context The Sergipe Basin in northeastern Brazil (Fig. 1) contains one of the most extensive marine Cretaceous carbonate successions among the central South Atlantic basins. The basin, which forms the southern part of the Sergipe-Alagoas Basin (Souza-Lima et al., 2002), is an elongate continental margin basin situated between latitudes 10°15′– 11°30′ S and longitudes 36°20′–37°30′ W. Onshore the basin is 16–50 km wide and 170 km long and covers an area of 6000 km2. The offshore portion comprises an area of c. 5000 km2.

According to Ojeda and Fugita (1976), structurally, the Sergipe Basin forms a half-graben with a regional dip averaging 10–15° to the southeast. The basin is bounded by faults with an overall NE–SW and NW–SE orientation, formed during the rupture of the African–South American continent in the early Cretaceous. The structural framework of the basin is characterized by large, tilted fault blocks, which form structural lows and highs. The Sergipe Basin belongs to the class of sedimentary basins characteristic of passive continental margins. According to Ojeda and Fugita (1976) and Ojeda (1982), the evolution of the basin comprises five main tectono-sedimentary phases, viz., intracratonic, pre-rift and rift phases (earliest Cretaceous to early Aptian), a transitional phase (Aptian), and an open-marine drift phase (late Aptian to Recent). The upper Aptian succession is represented by the upper part of the Muribeca Formation (Oiteirinhos Member) and the lower part of the Riachuelo Formation (Taquari and Angico members).

3. Material The stratigraphic succession studied here comprises parts of the Muribeca and Riachuelo formations (Fig. 2). In general, the Muribeca Formation represents evaporites and clastic and carbonate sediments deposited during the transitional phase. The Riachuelo Formation is a carbonate-dominated succession of calcareous mudstones and oolitic/ oncolitic and/or bioclastic grainstones or packstones, with subordinate conglomerates and sandstones (Angico Member), marls and shales (Taquari Member) (Koutsoukos et al., 1991), deposited during the openmarine drift phase. The material for this study derives from cores of two well sections, the Angico section (well GTP-17-SE, 70 samples) and the Taquari section (well GTP-24-SE, 108 samples), drilled by Petromisa/Petrobras (the Brazilian state-owned oil company). The wells are located on a W–E axis, extending from the Santa Rosa de Lima Low area (GTP-17SE, 10°39′ S and 37°10′ W) to the Aracaju High area (TaquariVassouras) (GTP-24- SE, 10°38′ S and 37°02′ W) (Fig. 2 cross section). The location on a W–E axis reflects a proximal-distal trend, with the Angico Member grading into the Taquari Member. In the Angico section (GTP-17-SE), the Riachuelo Formation is represented by the lower part of the Angico Member, consisting of alternating

Fig. 1. Location map of the continental margin basins of northeastern Brazil. (From Seeling, 1999).


545

Fig. 2. (A) Geological cross-section of the Muribeca and Riachuelo formations of the Sergipe Basin (adapted from Borchert, 1977). D = discontinuity according to Mendes (1994). Not to scale. (B) Lithostratigraphic scheme of wells GTP-17-SE (Angico section) and GTP-24-SE (Taquari section).

deposits of fine-grained sandstones and shales, and in the Taquari section (GTP-24-SE) by the lower part of the Taquari Member, consisting of alternating beds of calcareous mudstones and shales. The lower part of the Taquari section is dominated by calcareous mudstones and the upper part by shales (Fig. 2). The biostratigraphic data used in this study derive from the pollen zonation of Regali and Santos (1999) and Carvalho et al. (2016). The samples yielded an abundant and diverse palynoflora with assemblages typical of those reported from coeval beds of Brazilian continental margin basins (e.g. Dino, 1992; Rios-Netto, 2011). The Sergipea variverrucata Biozone was identified in the Taquari section (with the LAD of S. variverrucata at 42.7 m depth), indicating a late Aptian age for the section (Carvalho et al., 2016). In the Angico section, S. variverrucata was not recorded. However, the associated flora (e.g., Afropollis jardinus, Araucariacites australis, Bennettitaepollenites regaliae, Callialasporites segmentatus, Equisetosporites maculosus, Klukisporites foveolatus, Sergipea simplex) also indicates a late Aptian age.

palynological preparation compiled by Uesugui (1979), based on the methods developed by Erdtman (1943, 1969) and Faegri and Iversen (1966), among others. Mineral constituents were destroyed by hydrochloric and hydrofluoric acids before heavy-liquid separation. The remaining organic matter was sieved through a 10-μm mesh prior to mounting on slides. The palynological slides are kept in the palynology collection of the Museu Nacional, Universidade Federal do Rio de Janeiro. 4.2. Palynological analysis

4. Methods

After preparation, the samples were analysed under a transmitted light microscope. The quantitative analysis was based on the first 200 miospores (spores and pollen grains) counted on each slide. Marine elements (dinoflagellate cysts and microforaminiferal linings) were counted separately. Quantitative analyses of palynomorphs were performed on a total of 178 samples. Taxonomic identification was based on the works of Regali et al. (1975) and Dino (1992, 1994). The quantitative analysis was the basis for the establishment of the palynomorph distribution and the IndVal.

4.1. Sample preparation and processing

4.3. Indicator species analysis (IndVal)

Samples were processed at the Research Center of Petrobras (CENPES) in Rio de Janeiro using the standard Petrobras method for

Indicator species analysis (IndVal) (Dufrêne and Legendre, 1997) expresses whether species are characteristic of particular groups of

546


Fig. 3. Agglomerative, hierarchical clustering and stratigraphically constrained dendrogram (CONISS) of 70 samples from the Angico section showing the four intervals. Red dashed line indicates main break of the section.

samples (intervals). It is a simple method to find indicator species and species assemblages characterizing groups of sites. The analysis is assumed to reflect environmental conditions, which in turn is reflected in a sample of groups of units. The IndVal is determined on the basis of the formula proposed by Dufrêne and Legendre (1997), IndValGroup k, Species j = 100 × Ak,j × Bk,j, where Ak,j = specificity and Bk,j = fidelity, and the values obtained using the R package indicspecies (De Cáceres, 2013). In order to meet one of the criteria of IndVal, the ordination (typology) used here was cluster analysis, performed for both sections. The analyses, based on abundance and composition of miospores (spores and pollen grains), were employed using agglomerative, hierarchical clustering and stratigraphically constrained cluster analysis (CONISS) (Grimm, 1987) to establish groupings of samples. The results are displayed in dendrograms (Figs. 3 and 4).

Non-metric multidimensional scaling (NMDS) was performed on the basis of abundance data using the PAST software (Hammer et al., 2001) to attempt a correlation of the sections. The technique was chosen because the data matrix (depths/indicator species) is given for environmental variables, herein palaeoclimate phases. Moreover, the method is resistant to the effect of nonlinearity and heterogeneity of data.

5. Results The succession studied yielded a rich palynomorph assemblage dominated by gymnosperm pollen grains. However, fern spore taxa also show relatively high abundances, notably in the upper part of the sections. A total of 102 taxa were recorded, of which 43 in the Angico

Fig. 4. Agglomerative, hierarchical clustering and stratigraphically constrained dendrogram (CONISS) of 108 samples from the Taquari section showing the four intervals. Red dashed line indicates main break of the section.


547

Fig. 5. Indicator species of the studied sections: A) Classopollis classoides; B) Araucariacites australis; C) Cicatricosisporites sp.; D) Cicatricosisporites sp. E) Cicatricosisporites avnimelechi; F) Cicatricosisporites microstriatus; G) Verrucosisporites sp. H) Cyathidites sp.; I) Retitriletes sp.; J) Uesuguipollenites callosus; K) Callialasporites segmentatus; L) Bennettitaepollenites regaliae. Scale bars = 20 μm.

section (18 fern spores and 25 pollen grains) and 59 in the Taquari section (19 fern spores and 40 pollen grains). Sixty-six taxa (41 pollen grains and 25 fern spores) are common to both sections. The species Classopollis classoides (pollen grains) and Cicatricosisporites spp. (fern spores) dominate the samples of both sections (Appendices 1 and 2). 5.1. Typology (cluster analysis) Four main clusters are recognized in both sections, distinguished by cluster analysis (Figs. 3 and 4). The major break in both sections is strongly related to the relative abundance of Classopollis classoides pollen. For the Angico section, for clusters 1 and 2 together, the average of Classopollis classoides amounts to 79.5%, and for cluster 3 to 33.4%.

In the Taquari section, for clusters 1 and 2, the average of Classopollis classoides is 85.9%, and for clusters 3 and 4, 48.8%. 5.2. Indicator species analysis The indicator species analyses are strongly associated with particular intervals of the Angico and Taquari sections, even those with low abundances (e.g. Verrucosisporites spp.), as well as more abundant species, such as Classopollis classoides and Araucariacites australis (Fig. 5). IndVal for the Angico section indicates seven taxa associated with each interval revealed by cluster analysis (Table 1), viz., Classopollis classoides, Callialasporites segmentatus, Araucariacites australis, Cicatricosisporites avnimelechi, Verrucosisporites spp., Cicatricosisporites

548


Table 1 Indicator species values (IndVal) for the Angico section. Interval (I)

Indicator species

IndVal p (Monte Carlo) Significance level (0.05)

I1- 327.31–250.73 m I2 - 248.4–184 m

Classopollis classoides

0.581

0.001

Callialasporites segmentatus Cicatricosisporites avnimelechi Verrucosisporites spp. Cicatricosisporites microstriatus Araucariacites australis Cyathidites spp.

0.535 0.490

0.041 0.014

0.566 0.505

0.18 0.036

0.683 0.665

0.004 0.028

I3- 182.1–131.7 m

I4 - 125.5–18.0 m

The taxa are strongly associated with an interval established by CONISS.

microstriatus and Cyathidites spp. All indicator species are significantly associated with one interval (p b 0.05). IndVal for the Taquari section indicates nine taxa associated with the intervals revealed by cluster analysis (Table 2), viz., Classopollis classoides, Araucariacites australis, Uesuguipollenites callosus, Callialasporites segmentatus, Bennettitaepollenites regaliae, Cyathidites spp., Cicatricosisporites spp., Retitriletes spp. and Verrucosisporites spp.

5.3. Botanical affinities of the indicator species and environments In this study, the botanical affinities of the indicator species follow Regali et al. (1975), Tryon and Lugardon (1991), Dino (1992, 1994), Carvalho (2001, 2004), Antonioli (2001) and Rios-Netto et al. (2012) for spores and pollen grains. Cicatricosisporites is characterized by trilete spores with coarse, compact surfaces and often echinulate or granulate ridges. The main characteristics are the parallel ridges. According to Tryon and Lugardon (1991), fossil spores are more elaborate than those of extant genera, particularly in the Cretaceous, and the family was more abundant and widely distributed. The spores of Cicatricosisporites, previously assigned to the family Schizaeaceae, are now assigned to the family Anemiaceae of the order Schizaeales (Smith et al., 2006), with only one genus: Anemia. Anemiaceae is one of the most ancient extant fern families (Labiak et al., 2015), and Cicatricosisporites type spores were ancestral for the clade comprising living Anemiaceae and Schizaeaceae. The genus occurs mainly in coastal regions of tropical and subtropical America (Tryon and Tryon, 1982; Narváez et al., 2013). However, Anemia is also recorded in the highlands

Table 2 Indicator species values (IndVal) for the Taquari section. Interval (I)

Species

I1 - 252.6–178.56 m Classopollis classoides I2 - 170.43–146.43 Uesuguipollenites callosus m Callialasporites segmentatus Bennettitaepollenites regaliae Cyathidites spp. Cicatricosisporites spp. Araucariacites australis I3 - 135.75–77.2 m Retitriletes spp. I4 - 75.4–13.25 m Araucariacites australis Verrucosisporites spp.

IndVal p (Monte Carlo) Significance level (0.05) 0.713 0.910 0.886

0.001 0.001 0.001

0.804

0.001

0.779 0.700 0.675 0.609 0.605 0.538

0.001 0.002 0.006 0.005 0.005 0.029

The taxa are strongly associated with an interval established by CONISS.

of northeastern Brazil (Dino, 1992). According to Dettmann and Clifford (1992), Anemia appeared in the Late Jurassic in the latitudes of northern Gondwana–southern Laurasia. Cyathidites is a form genus of trilete psilate spores, with a concavely triangular to subcircular outline. Although characteristic of several modern and extinct families, our taxa were probably produced by the tree fern family Cyatheaceae. The genus belongs to the arborescent plants of the family Cyatheaceae. According to Tryon and Lugardon (1991) the extant and fossil representatives occur mainly in tropical montane areas. In northeastern Brazil, extant Cyatheaceae live in shaded habitats of the mountain forests (Dino, 1992). Carvalho (2004) identified four associations in the Riachuelo Formation (Taquari and Angico members), based on cluster analyses. Cyathidites is grouped in the same association as upland elements (e.g. Calliallaspollenites, Araucariacites) and many genera of spores (e.g. Verrucosisporites, Cicatricosisporites). Retitriletes encompasses trilete spores with circular ambs and coarsely reticulate sculpture (Nichols, 2002). Reticulate spores are often associated with members of the extant family Lycopodiaceae, which includes four genera (Tryon and Lugardon, 1991). Retitriletes recorded in this study is similar to the modern genus Lycopodium, which today is found worldwide. Verrucosisporites comprises trilete spores with circular ambs and verrucate, low turberculate to papillate surface sculpture. Our taxa resemble those produced by the family Osmundaceae (e.g., Dino, 1992; Mego and Prámparo, 2013), a primitive group between eusporangiate and leptosporangiate ferns recorded since the Late Permian (Taylor et al., 2009). Today, the family, with its three genera Leptopteris, Osmunda and Todea (Smith et al., 2006), inhabits tropical and temperate regions, preferably in dense forests and rain forests. In general, these plants have a terrestrial or marshy habitat, rarely arborescent (Dino, 1992). The family Araucariaceae today has a dominantly austral distribution; by contrast, during the Mesozoic, the family was distributed in both the northern and southern hemispheres (Dutra and Stranz, 2003). Most modern representatives of the family Araucariaceae live in sites under a subtropical or temperate mesothermic climate (Strahler and Strahler, 1989; Nimer, 1990; Dutra and Stranz, 2003), near but not at sea level. However, there are exceptions, as is the case of the species Araucaria araucana (Mol.) Koch, which lives in dry and rigorous winters of the Andes (Dutra and Stranz, 2003). According to Kunzmann (2007), the Araucariaceae had their widest distribution during the Cretaceous. The family was typical of highlands and related to a tropically centred group, whose pollen spacies found in lowland deposits of early Cretaceous age (Doyle et al., 1982). Araucariacites and Callialasporites have been assigned to the family Araucariaceae (e.g. Dino, 1992; Dutra and Stranz, 2003; Gary et al., 2009). However, Callialasporites has mainly been assigned to the family Podocarpaceae (Archangelsky and Gamerro, 1967; Anderson et al., 2007; Dutra et al., 2007; Maizatto et al., 2009). Araucariacites are spherical non-aperturate grains with granular exines. Callialasporites pollen are monosaccates or sometimes divided into three (pseudotrisaccate), with a spherical outline and generally with a psilate wall. Bennettitaepollenites is a monosulcate pollen grain, with a fusiform outline and psilate wall. The aperture is highly distinctive, crossing the entire longitudinal surface. Bennettitaepollenites is assigned to the Bennettitales, which extends from the Triassic to the Cretaceous and occurs in both hemispheres (Dino, 1992). Bennettitales reached its apogee in the Aptian and is usually associated with hot climates (Dino, 1992; Antonioli, 2001). Classopollis has a spherical outline and is monoporate with a subequatorial rimula. It is commonly found in tetrads in the upper Aptian of most of the continental margin basins of the South Atlantic and assigned to warmth-loving conifers of the family Cheirolepidiaceae (Alvin, 1982). Classopollis occurs in mainly lagoonal and marine nearshore environments, often associated with evaporites (Batten, 1975; Vakhrameev, 1970, 1981; Doyle et al., 1982; Hashimoto, 1995; Heimhofer et al., 2008). These pollen grains were elements of a


549

Table 3 Pearson correlation of indicator species for the Angico section. Indicator species


Callialasporites segmentatus

Cicatricosisporites avnimelechi

Verrucosisporites spp.

Cicatricosisporites microstriatus

Araucariacites autralis

Cyathidites spp.

Marine elements

-0,13

-0,01

-0,33

-0,10

-0,71

-0,44

-0,20

0,28

-0,06

0,15

0,27

0,04

-0,02

-0,10

0,22

0,11

-0,08

-0,09

0,24

0,20

0,61

0,28

0,08

0,27

-0,01

0,29

0,19

Classopollis classoides Callialasporites segmentatus

-0,13

Cicatricosisporites avnimelechi

-0,01

0,28

Verrucosisporites spp.

-0,33

-0,06

-0,10


-0,10

0,15

0,22

0,24

Araucariacites autralis

-0,71

0,27

0,11

0,20

Cyathidites spp.

-0,44

0,04

-0,08

0,61

0,27

0,29

Marine elements

-0,20

-0,02

-0,09

0,28

-0,01

0,19

0,08

0,36 0,36

Marked correlations are significant at p b 0.05000 (blue for positive and red for negative correlations).

xerophytic flora present in most South American and African basins (e.g. Schrank and Mahmoud, 1998; Carvalho, 2004). Uesuguipollenites is an inaperturate pollen grain with scabrate ornamentation, circular outline and a central circular thickening. Dino (1992, 1994) associated Uesuguipollenites with the families Taxaceae or Cupressaceae. Generally, these two families are associated with a temperate climate. Therefore, Uesuguipollenites is associated with upland floras. Carvalho (2004) identified four palynological associations for the Taquari section, based on cluster analyses. Useguipollenites is grouped in the same association as Calliallaspollenites, Araucariacites and many genera of spores (e.g. Cyathidites, Verrucosisporites, Cicatricosisporites).

As shown in Tables 3 and 4, the Pearson coefficient emphasizes the change from a Classopollis to an Araucariacites and fern spore flora, as well as a significant negative correlation of Classopollis classoides with Cyathidites spp. and Verrucosisporites spp., in particular with Araucariacites australis. This implies that in arid conditions, the Classopollis flora dominated the palaeoenvironment. This flora also shows a negative correlation with marine elements for both sections studied. The negative correlation is more evident in the Taquari section, which shows a greater marine influence than the Angico section. Elements of the upland flora, represented by Araucariacites australis, Uesuguipollenites callosus, Callialasporites segmentatus and Cyathidites spp., show a positive correlation with each other and with other fern spores (e.g. Cicatricosisporites spp., Verrucosisporites spp.) (Tables 3–4).

5.4. Relationships among indicator species 6. Palaeoclimatic interpretation The Pearson coefficient (+/− 1) obtained from the relative abundance of indicator species and marine elements (dinocysts and microforaminiferal linings) was used to yield a correlation matrix and to identify the relationships among the indicator taxa (Tables 3 and 4).

The flora recorded in upper Aptian rocks of South America and Africa is typical of warm conditions and commonly associated with semi-arid to arid climate (e.g., Brenner, 1976; Schrank and Mahmoud, 1998;

Table 4 Pearson correlation of indicator species for the Taquari section. Indicator species Classopollis classoides Uesuguipollenites callosus Callialasporites segmentatus Bennettitaepollenites regaliae Cyathidites spp. Cicatricosisporites spp. Retitriletes spp. Araucariacites australis Verrucosisporites spp. Marine elements


Uesuguipollenites callosus


Bennettitaepollenites regaliae

Cyathidites spp.

Cicatricosisporites spp.

0,08

0,02

0,08

-0,15

0,09

0,11

-0,13

-0,21

-0,39

0,70

0,58

0,24

0,45

-0,01

0,33

-0,05

0,09

0,64

0,41

0,55

0,01

0,48

0,13

0,06

0,08 0,02

0,70

0,30

0,08

0,58

0,64

-0,15

0,24

0,41

0,30

0,09

0,45

0,55

0,41

0,46

Retitriletes Araucariacites Verrucosisporites Marine spp. australis spp. elements

0,41

0,01

0,30

-0,02

0,03

0,46

-0,05

0,37

0,31

0,18

0,22

0,57

0,36

0,00

0,11

-0,01

0,01

0,01

-0,05

0,22

-0,13

0,33

0,48

0,30

0,37

0,57

0,15

-0,21

-0,05

0,13

-0,02

0,31

0,36

0,10

0,46

-0,39

0,09

0,06

0,03

0,18

0,00

0,00

-0,02

Marked correlations are significant at p b 0.05000 (blue for positive and red for negative correlations).

0,15

0,10

0,00

0,46

-0,02 0,07

0,07

550


Angico section Classopollis classoides


Cicatricosisporites Verrucosisporites avnimelechi spp.


Araucariacites australis

Cyathidites spp.

Intervals (IndVal)

18 38

AS-4

78 98 118 138

Wet phase

58

AS-3

158 178 198

238 258 278

AS-1

298

Dry phase

AS-2

218

318 0

100

200 0.0

2.0

4.00.0

2.5

5.0

2.0

4.0

6.0

0.0

1.5

3.0

75

150 0

24

48

100

Fig. 6. Stratigraphic distribution of indicator species from the Angico section showing the dry and wet phases. Dashed line = average values.

Carvalho, 2004; Heimhofer et al., 2012). In both sections studied here, a dry and a wet phase are recognized.

6.1. Dry phase The dry phase is characterized by a conspicuous dominance of Classopollis classoides. The phase is recognized in both sections studied. In the Angico section, the phase is subdivided into the intervals AS-1, associated with C. classoides, and AS-2, associated with Callialasporites segmentatus and Cicatricosisporites avnimelechi (Fig. 6). In the Taquari section, only one dry interval, TS-1, is recognized, also strongly associated with C. classoides (Fig. 7). In the AS-1 interval, C. classoides, including its tetrads, is dominant. Peaks of Callialasporites segmentatus are recorded (Fig. 6). In the TS-1 interval, the flora shows the same pattern as in AS-1, i.e., a high abundance of C. classoides, although with a conspicuous decreasing trend upwards (Fig. 7). The dominance of C. classoides suggests that dry conditions prevailed during the TS-1 interval, which is also implied by the rare occurrence of other indicators (e.g., spores). Warmth-loving conifers of the family Cheirolepidiaceae and their Classopollis pollen occurred mainly in lagoonal and marine nearshore environments and are often associated with evaporites (Vakhrameev, 1970, 1981; Doyle et al., 1982; Hashimoto, 1995). They were elements of a xerophytic flora present in most South American and African basins (e.g., Schrank and Mahmoud, 1998; Carvalho, 2004). According to Dino (1992), the Cheirolepidiaceae reached their peak in the arid belt, where they preferred tropical to subtropical climates, with somewhat dry conditions. These conifers grew not only along the coast, but also inland and on plains and slopes of the highlands.

Herngreen and Chlonova (1981) proposed that the early Cretaceous sedimentary basins of northeastern Brazil belong to the pre-Albian West African–South American microfloral province (WASA), which is equivalent to the Northern Gondwana province of Brenner (1976), characterized by a predominance of Classopollis and Araucariacites. The results achieved here support this proposal, although with Classopollis indicating a drier phase. The AS-2 interval shows a high abundance of upland flora represented by Callialasporites segmentatus and small quantities of fern spores (e.g. Cicatricosisporites avnimelechi, Cicatricosisporites microstriatus) (Fig. 6). The co-occurrence of Classopollis and Callialasporites has been reported frequently (e.g. Dino, 1992; Carvalho, 2004; Volkheimer et al., 2015). In this study, this co-occurrence may indicate transitions between dry and wet phases supported by the presence of ferns. This could also represent a phase of high relief under dry climate, with Classopollis being dominant in the lowlands and Araucariaceae or Podocarpaceae (Callialasporites) in the uplands. Studies indicate that some Cicatricosisporites were tolerant of arid climate (e.g. Duarte et al., 2015). Thus, available data suggest that the persistence of Classopollis and increases in upland and fern spores indicate arid or semi-arid climate with nearby elevated areas and bodies of fresh water (Dino, 1992; Volkheimer et al., 2008, 2015). 6.2. Wet phase A pronounced change in vegetation occurred with the increase in ferns and upland flora, particularly Araucariacites (Figs. 6 and 7). This taxon, traditionally attributed to the family Araucariaceae, is the second most abundant among the terrestrial palynomorphs and belongs to the upland flora.


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Fig. 7. Stratigraphic distribution of indicator species from the Taquari section showing the dry and wet phases. Dashed line = average values.

Vakhrameev (1981) and Doyle et al. (1982) concluded that an increase in aridity resulted in a decline of Araucariacites. This flora is typical of warm and wet climates in the late Aptian of South America and Africa (Batten, 1984; Dutra and Stranz, 2003), which may explain its association with fern spores. Another possibility, which complements this concept, is presented by Chaboureau et al. (2012), who argue that precipitation induced by orographic effects provided an increase both in upland flora (Araucariacites) and in lowland flora (ferns). In their palynological studies of the Holocene of southern Brazil, Iriarte and Behling (2007) found a significant expansion of Araucaria, based on the increasing abundance of its pollen, which they attributed to an increase in precipitation. Kujau et al. (2013) also reported the same phenomenon in the Valanginian, i.e., an increase in ferns and Araucariacites flora concomitant with a decrease in Classopollis classoides, which they attributed to increased humidity. The indicator species of ferns (Verrucosisporites spp., Cyathidites spp. and Cicatricosisporites spp.), together with the upland flora represented primarily by Araucariacites, are strongly associated with the wet phase and together replaced the Classopollis flora. Studies of Deep Sea Drilling Project sites (Harris, 1977; Davey, 1978; McLachlan and Pieterse, 1978; Morgan, 1978; Kotova, 1983) suggest that the abundance of Classopollis and other xerophyte palynomorphs shows strong fluctuations, with a decreasing trend towards the uppermost Aptian, correlated with an increase in the abundance of fern spores. Fern spores are common in the upper Aptian of the Brazilian basins (Carvalho, 2004; Carvalho et al., 2006a). As ferns depend on water to

reproduce, they are generally associated with moist conditions and, consequently, rarely reported from arid environments. Mejia-Velasquez et al. (2012) studied the Aptian–Albian interval of southwestern central Colombia and also used the abundance and diversity of fern spores as an indicator of humidity comparing with Classopollis occurrence. Their study, however, makes no mention of the relation between upland flora with fern spores. The wet phase is subdivided into the intervals AS-3 and AS-4 for the Angico section and TS-2, TS-3 and TS-4 for the Taquari section. In the AS-3 and AS-4 intervals, Verrucosisporites spp./Cicatricosisporites microstriatus and Araucariacites australis/Cyathidites spp. dominate (Figs. 6–7). The first interval associated with the wet phase in the Angico section (AS-3), shows persistent high abundance of Classopollis classoides (Fig. 6), especially at the onset of the interval. In the AS-3 interval, the most significant indicator species are the fern spores Verrucosisporites spp., Cicatricosisporites microstriatus and Cyathidites spp. (Table 2), indicating wet conditions. The indicator species for the AS-4 interval is Araucariacites australis. High abundances of this taxon are recorded concomitant with the lowest abundance of Classopollis classoides. The most significant indicator species of fern spores persist in this interval (Fig. 6). In the Taquari section, the indicator species typical of the upland flora, e.g., Uesuguipollenites callosus, Callialasporites segmentatus, Araucariacites australis and Cyathidites spp., are strongly associated with TS-2, the first wet interval (Fig. 7). An increasing abundance of upland flora and the proportional increase in indicator species of the ferns Cicatricosisporites spp. and Verrucosisporites spp. suggest that the TS-2

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Fig. 8. Non-metric multidimensional scaling analysis (NMDS) plots for the Angico and Taquari sections. A) Samples grouped according to dominance of Classopollis, Araucariacites spores and fern spores. B) Samples grouped according to paleoclimatic phases. C) Correlation between the palaeoclimatic phases of the Angico and Taquari sections.


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Fig. 9. Reconstruction of dry and wet scenarios in the Sergipe Basin during the Aptian, based on distributions of the main plant group. SOURCE: Image by Victor Feijó.

interval became more humid. Also, in this interval the highest number of indicator species is recorded (Table 2), all associated with more humid conditions. These species are Uesuguipollenites callosus, Callialasporites segmentatus, Araucariacites australis, and Cyathidites spp. associated with upland flora and Cicatricosisporites spp. and Verrucosisporites spp., which are derived from parent plants associated with lowland settings near bodies of freshwater. Duarte et al. (2015) analysed samples from a number of Brazilian sedimentary basins and concluded that species of Cicatricosisporites are abundant and diversified, indicate moderately humid climate, and

are often associated with other spores. Where they are associated with elements typical of arid climate (e.g., Classopollis), they show insignificant proportions. A sudden increase in Classopollis classoides is recorded in the TS-3 interval. The increase in this xerophytic flora in response to a change to drier conditions probably caused a decrease in upland flora (e.g., Uesuguipollenites callosus, Callialasporites segmentatus, and Araucariacites australis) (Fig. 7). However, the abundance of C. classoides decreases towards the top of the interval, which corresponds to an increase in fern spores and Araucariacites australis.

Fig. 10. Correlation between palaeoclimatic phases of the Angico and Taquari sections using NDMS first axis and marine elements. Dashed line = average values.

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Fig. 11. Idealized palaeoclimatic and palaeoceanographic setting for the late Aptian in the South Atlantic after Chaboureau et al. (2012), Hay and Floegel (2012) and Carvalho et al. (2016), showing the Sergipe Basin. Reconstruction at 116 Ma modified from ODSN Plate Tectonic Reconstruction Service.

The dominance of fern spores and upland flora continues into the TS3 interval, indicating that more humid conditions remained. However, there was a decline in Uesuguipollenites callosus and Callialasporites segmentatus, whereas the abundance of Araucariacites australis continued high. The association of Retitriletes spp. and other fern spores (Cicatricosisporites spp., Verrucosisporites spp.) in the TS-3 interval (Fig. 7), as also observed in TS-2, implies a persistence of more humid conditions. In the TS-4 interval, the dendrogram (Fig. 4) shows two clusters. However, in both clusters, the indicator species Araucariacites australis is abundant (Fig. 7). The predominance of A. australis continuing into this part of the succession indicates the persistence of humid conditions. This corresponds to the lowest abundances of Classopollis classoides in the Taquari section, which are probably a result of increasingly humid conditions. Fern spores are represented mainly by Verrucosisporites spp.

6.3. Relationships between the sections The distribution curves of indicator species for the Angico and Taquari sections show consistent patterns in the changes in vegetation during the late Aptian. The nature of the changes seems to be the same for the two sections. The stratigraphical distribution of the indicator species (Figs. 6 and 7) shows that the xerophytic flora (Classopollis) declined markedly at the 180 m level in both sections and is replaced by a flora typical of humid environments (Araucariacites and ferns). However, the sections are slightly different, with Taquari being more marine than Angico (Carvalho, 2001; Carvalho et al., 2006a). Therefore, the Classopollis flora that is typical of lagoonal and marine nearshore environments in this Aptian interval is most evident in the Angico section (AS-1 interval), where the abundance curve of C. classoides drops below the general average (124.6, Appendix 2) only three times, and


no decreasing trend is observed (Fig. 6). Thus, the transition from the dry to the wet phase is abrupt in the Angico section and gradual in the Taquari section (Fig. 7). On the basis of the indicator species of the two sections, we used NMDS to attempt a comparison of the intervals (Fig. 8A–B). The plot shows a distinct distribution between the intervals (Fig. 7); however, the intervals dominated by Classopollis (AS-1, AS-2 and TS-1) show a high degree of grouping, in the same way that the Araucariacites and fern spores dominate (Fig. 8A). The peaks of coincident indicator species for the two sections (Classopollis classoides, Callialasporites segmentatus, Araucariacites australis) show that, in general, the four intervals are strongly coincident (i.e., AS-1 and TS-1, AS-2 and TS-2, AS-3 and TS-3, AS-4 and TS-4) (Fig. 8B–C). The intervals coincide satisfactorily, except for AS-2 and TS-2, because the C. classoides abundance is higher in AS-2 than in TS-2. We attribute these differences to the higher terrigenous influence in AS-2. The Classopollis record suggests that the Angico section was deposited during a dry phase, which remained constant for approximately 138 m of section and was more persistent than in the Taquari section (approximately 60 m) (Fig. 9A, dry scenario). After the dry phase, represented by the intervals AS-1–2 and TS-1, the vegetation indicates a wet phase (upland flora and ferns) persisting until the top of the sections, varying in composition and abundance in response to climatic forcing and sea-level changes (Fig. 9B, wet scenario). The intervals assigned to wet conditions, intervals AS-3–4 and TS-2– 4, show strong correlations. 6.4. Causes of climate changes The replacement of Classopollis by the Araucariacites and fern flora reflects a change from dry to wet conditions. Changes in floral composition were also assessed through correspondence analysis (CA) using the PAST software (Hammer et al., 2001). The analysis shows an abrupt change in flora from intervals AS-2 and TS-2 in the sections (Figure 10) (see Figs. 3 and 4), indicating that there was a significant change from a Classopollis to an Araucariacites flora. This change is evident in both sections and indicates an increase in humidity. Weissert et al. (1998) suggested that an increasingly zonal climate pattern was established along the opening Atlantic–Tethys seaway in the early Cretaceous, and that major rainfall belts were shifted into equatorial regions. It is possible that the increasing humidity in the equatorial belt is a result of cooling in the North Atlantic. Maps of climatic zones published by Chumakov et al. (1995) have served as the basis for studies of the climatic evolution during the Cretaceous (e.g., Skelton et al., 2003; Hay and Floegel, 2012). For South America, a humid belt is suggested from the Albian to Maastrichtian. However, because of the absence of fossil indicators of humidity for the Berriasian and Aptian, the humid belt is not indicated on the map. However, as pointed out by Hay and Floegel (2012), the idea of an equatorial region without humidity is untenable. The humid belt in the palaeoequator region is interpreted as analogous of the present Intertropical Convergence Zone (ITCZ) (Hay and Floegel, 2012). Using experiments of the Fast Ocean Atmosphere Model (FOAM) for the Aptian of the South Atlantic, Chaboureau et al. (2012) suggested that the Sergipe Basin area was affected by strong rainfall seasonality driven by the latitudinal shift of the ITCZ. Intense rainfall occurred during the austral spring, summer and autumn due to this shift across the equatorial areas. The Sergipe Basin was located below the ITCZ and characterized by high precipitation, up to 12 to 14 mm per day, with seasonal rainfall due to the movement of the ITCZ, and pronounced dry and wet seasons (Fig. 11). It appears, thus, that the seasonal shifts of the ITCZ defined the latitudinal boundaries of wet and dry areas. The overall increase in humidity in the studied sections is concomitant with an increase in marine influence indicated by the dinoflagellate

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cysts and microforaminiferal linings (Fig. 9). Studies show that the increase in marine elements is related to the first major flooding surface observed in the upper Aptian in the continental-margin basins of Brazil (e.g., Azevedo, 2004; Arai, 2005, 2007, 2009, 2014; Carvalho et al., 2006a, 2006b, 2016). According to Kujau et al. (2013), changes in composition and abundance of palynomorphs in the sedimentary record reflect not only the vegetation of a particular area, but are also influenced by changes in sea level. Rises in sea level reduce the coastal plains, and thus, plants adapted to these environments are reduced. This reduction is in the present study indicated by the decrease in abundance of Classopollis classoides. The results of the Pearson coefficient (Tables 3 and 4) support this observation, showing a negative correlation between marine elements and Classopollis, particularly in the Taquari section. In the flora associated with a wet phase, only two elements, Verrucosisporites spp. and Cyathidites spp., show a positive correlation, both in the Angico section. However, other elements show no significant negative values. It should be noted that with the rise of sea level, the Taquari section became more distant from land, which probably resulted in a decreasing input of landderived, especially fern spores. The rising sea level probably enabled the development of lowland humid environments and, thus, the spread of ferns. The warmer climate also led to increased humidity. Li et al. (2000), studying late Cretaceous deposits of Tunisia, associated warm/humid climates with high sea levels and less humid climates with low sea levels. As the South Atlantic rift progressively expanded, the sea transgressed from the central North Atlantic across the northern part of South America from the late Aptian to the late Albian (Koutsoukos et al., 1991). The general rise in sea level from the late Aptian may have played a role in the development of humid conditions in the South Atlantic. 7. Conclusions • The upper Aptian successions in the Angico and Taquari sections contain well-preserved, taxonomically diversified palynomorph assemblages, dominated by the genera Classopollis and Araucariacites. Less common taxa include fern spores of Cicatricosisporites and Verrucosisporites. Taxa identified by indicator species analysis (IndVal): Araucariacites australis, Bennettitaepollenites regaliae, Callialasporites segmentatus, Cicatricosisporites avnimelechi, Cicatricosisporites microstriatus, Cicatricosisporites spp., Classopollis classoides, Cyathidites spp., Retitriletes spp. Uesuguipollenites callosus, and Verrucosisporites spp. • A dry and a wet phase are identified in the sections based on the palynomorph content. The dry phase is characterized by significant abundance and low variance of Classopollis classoides. The wet phase is characterized by high abundances of Araucariacites australis and the fern spores Cicatricosisporites spp. and Verrucosisporites spp. • Negative correlation between the two main floras, Classopollis and Araucariacites with fern spores, mirrors their different climatic preferences and thus different ecological conditions for the dry and wet phases. • The change from the Classopollis to the Araucariacites flora may be caused by a shift of the Intertropical Convergence Climatic Zone (ITCZ) during a relative sea-level rise. Acknowledgments We express our thanks to Petrobras for giving M.A. Carvalho the opportunity to study the material. This study was funded mainly by the Brazilian National Council for Scientific and Technological Development (grant no. 301573/2013-1) (Conselho Nacional de Desenvolvimento

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Científico e Tecnológico (CNPq)), the Brazilian Research Funding Organization (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), grant no. BEX 11616/13-0) and the German Academic Exchange Service (DAAD, grant no. A/13/03339). The authors thank Appendix 1

Lana Sylvestre (UFRJ, Rio de Janeiro) for solving taxonomic issues about the ferns. We also thank James Doyle (UC Davis), Jennifer Galloway (Carleton University, Calgary) and two anonymous reviewers for helpful suggestions.

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Appendix 2

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Appendix 2 (continued)

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