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New plant fossils from the Lower Cretaceous of the Parnaíba Basin, Northeastern Brazil: Southern Laurasia links

ABSTRACT:

This study reports on the presence of a diverse set of gymnosperm and angiosperm macrofossils from the Codó Formation, Parnaíba Basin, whose assemblage was previously known only by the occurrence of pollen grains, spores, wood fragments, leaves and roots associated with Nympheaceae. In the Brejo municipality, northeastern Maranhão State, marl levels attest a transitional to marginal lacustrine environment, with occasional marine ingressions, demonstrated by the presence of crustaceans, gastropods and fishes. The plant fossils are preserved exclusively by molds and impressions, and its diversity is represented by few specimens, suggesting taphonomic processes of selection and transportation. The taphoflora is composed of Gnetales (?Drewria), conifers (Cupressinocladus and Brachyphyllum), and basal angiosperms (Nympheales, Magnollids, and/or basal Eudicots), which support an upper Aptian - ?Albian age. It displays affinities with both the well-known flora of the Araripe Basin (Santana Formation) as well as those ones identified in deposits from the south of North America (Potomac Group), suggesting that terrestrial links persisted in the equatorial areas of the Pangea at the end of the Early Cretaceous.

KEYWORDS:
Lower Cretaceous; Macroflora; Parnaíba Basin; Codó Formation

INTRODUCTION

In the beginning of the Cretaceous, ferns and gymnosperms dominated the plant communities of a broad equatorial paleofloristic province. At that time, the province included a large part of the modern landmasses of South Hemisphere and southern Laurasia, characterized by assemblages containing elater-bearing pollen grains (Willis & McElwain 2002Willis K.J., & McElwain J.C. 2002. The evolution of plants. Oxford, Oxford University Press, 287 p., Vallati 2013Vallati P. 2013. Paleotropical pollen grains from the Neuquén Group, Patagonia, Argentina. Carnets de Géologie [Notebooks on Geology], L05:273-279.). Tropical, warm, and dry, conditions influenced the climate in this equatorial realm (Vakhrameev 1991Vakhrameev V.A. 1991. Jurassic and Cretaceous floras and climates of the Earth. Cambridge: Cambridge University Press, 318 p. ).

The Lower Cretaceous floras in Northeastern Brazil (Araripe, Parnaíba, Tucano, Sanfranciscana and Sergipe-Alagoas basins) allow us to infer halophytic forms growing in a xeromorphic vegetation, dominated by conifers and Gnetales, with Bennettitales, Caytoniales, Pteridospermales and early angiosperms as a minor component (Regali et al. 1974Regali M.S.P., Uesugui N., Santos A.S. 1974. Palinologia dos sedimentos meso-cenozóicos do Brasil (I). Boletim Técnico da Petrobras, 17(3):177-191., Lima 1982Lima M.R. 1982. Palinologia da Formação Codó na região de Codó. Boletim Instituto de Geociências da USP, 13:116-128., Kunzmann et al. 2006Kunzmann L., Mohr B., Bernardes-de-Oliveira M.E.C., Wilde V. 2006. Gymnosperms from the Lower Cretaceous Crato Formation (Brazil). II. Cheirolepidiaceae. Fossil Record, 9:213-225. DOI: 10.1002/mmng.200600009
https://doi.org/10.1002/mmng.200600009...
, Bernardes-de-Oliveira et al. 2007Bernardes-de-Oliveira M.E.C., Mohr B., Dino R., Guerra-Sommer M. 2007. As floras mesofíticas brasileiras no cenário paleoflorístico mundial In: Carvalho I.S., Cassab R.C.T., Schwanke C., Carvalho M.A., Fernandes A.C.S., Rodrigues M.A.C., Carvalho M.S.S., Arai M., Oliveira M.E.Q. (eds.). Paleontologia: Cenários de Vida. Rio de Janeiro, Interciência, v. 1, p. 203-241., Mohr et al. 2007Mohr B., Bernardes-de-Oliveira M.E.C., Loveridge R.F. 2007. The macrophyte flora of the Crato Formation In: Martill D.M., Bechly G., Loveridge R.F. (eds.). The Crato Fossil Beds of Brazil. New York, Cambridge University Press, p. 537-565.).

For the Codó Formation, Parnaíba Basin, previous works have only reported the presence of angiosperm wood logs and indeterminate leaves and roots (Moraes Rego 1923Moraes Rego L.F. 1923. Reconhecimento geológico feito no estado do Maranhão. Relatório Anual do Diretor. Serviço Geológico e Mineralógico, p. 74-77., Borges 1937Borges J. 1937. Estudos geológicos nos estados do Maranhão e Piauhy. Relatorio Annual. Rio de Janeiro, Serviço Geológico e Mineralógico., Duarte 1959Duarte L. 1959. Relatório da seção de paleontologia. Relatório Anual do Diretor. Rio de Janeiro, DGM/DNPM, p. 167-194.), which Duarte and Santos (1993Duarte L., & Santos R.S. 1993. Plant and fish megafossils from the Codó Formation, Parnaíba Basin, NE Brazil. Cretaceous Research, 14:735-746. https://doi.org/10.1006/cres.1993.1049
https://doi.org/10.1006/cres.1993.1049...
) assigned to a new species, Nymphaeites choffati (= Klitzschophyllites choffati). The fossil wood log, Lecythioxylon brasiliense Milanez, comes from outcropping at the margin of Parnaíba river, in Piauí State, considered correlate with those of the Codó Formation (Milanez 1935Milanez F.R. 1935. Estudo de um dicotyledoneo fossil do Cretaceo. Rodriguésia, 1:82-89.).

The palynological assemblage of the Codó Formation, firstly studied by Lima (1982Lima M.R. 1982. Palinologia da Formação Codó na região de Codó. Boletim Instituto de Geociências da USP, 13:116-128.), attests to a flora dominated by Gnetales pollen grains (Equisetosporites, Singhia, Gnetaceaepollenites and Steevesipollenites), followed in number by conifers (Classopolis spp., Araucariacites spp. and Exesipollenites tumulus), and angiosperms (Afropollis (Reticulatosporites) jardinus). Still little represented (and absent until now in the macroflora), the pteridophytes are diversified, with specimens related to the Cyatheaceae, Dicksoniaceae and Osmundaceae. The presence of Sergipea has supported part of the Codó Formation deposits in the Aptian biozone Sergipea variverrucata (Pedrão et al. 1996Pedrão E., Barrilari I.M.R., Lima H.P. 1996. Palynological studies in the Cretaceous of the Parnaíba basin. In: Congresso Brasileiro de Geologia, 39. Annals… Salvador, Sociedade Brasileira de Geologia, p. 380-383., Regali & Santos 1999Regali M.S.P., & Santos P.R.S. 1999. Palinoestratigrafia e geocronologia dos sedimentos Albo-Aptianos das bacias de Sergipe e de Alagoas. In: Simpósio sobre o Cretáceo do Brasil, 1. Abstract, p. 411-419., Antonioli 2001Antonioli L. 2001. Estudo palino-cronoestratigráfico da Formação Codó - Cretáceo Inferior do Nordeste Brasileiro. Thesis. Instituto de Geologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, 265 p., Maizatto et al. 2011Maizatto J.R., Queiroz-Neto J.V., Ferreira E.P., Bahniuk A. 2011. Palinomorfos e ostracodes não-marinhos de afloramento da Formação Codó, Bacia do Parnaíba. In: Carvalho I.S., Srivastava N.K., Strohschoen Júnior O., Lana C.C. (eds.). Paleontologia: Cenários de Vida. Rio de Janeiro, Interciência , v. 3, p. 367-e377.).

In Brejo County, State of Maranhão, focus of this study, the fossil plants occur in limestone beds exposed in open pit mines at two locations: Faveirinha Quarry and Perneta Ranch (Fig. 1), where the occurrence of conifers, Gnetales and angiosperms were preliminarily reported by Lindoso et al. (2011Lindoso R.M., Carvalho I.S., Medeiros M.A., Pereira A.A., Santos R.A.B., Mendes I.D., Brito J.M., Bôas I.V., Araújo M.N., Ferreira N.N. 2011. Novos sítios fossilíferos em carbonatos da Formação Codó (Aptiano-Albiano) da Bacia do Parnaíba, Maranhão, Brasil In: Carvalho I.S., Srivastava N.K., Strohschoen Jr. O.S., Lana C.C. (eds.). Paleontologia: Cenários de Vida. Rio de Janeiro, Interciência , p. 819-827., 2013aLindoso R.M., Carvalho I.S., Medeiros M.A., Mendes I.D., Marques N.E., Brito R., Almeida C.M. 2013a. A megaflora da Formação Codó (Aptiano, Bacia do Parnaíba), nordeste do Brasil. In: 23º Congresso Brasileiro de Paleontologia, 23., Gramado. Annals... Gramado, SBP, p. 175-176.).

Figure 1:
The location is Brejo County, Maranhão State, northeastern Brazil. The black stars indicate the two quarries where the plant fossils were collected.

The present study aims to describe these new materials and analyze their relationship with the previously known taxa of other paleo-equatorial basins. Since some of the morphotypes are poorly represented, and others refer to isolate leaves and apical shoots, without associated reproductive structures, its description and illustration try to evaluate their diversity and compare them with other Early Cretaceous floras. With this process, we also intend to make possible inferences based on paleoecology, paleogeology and age.

GEOLOGICAL SETTING

The Parnaíba Basin spreads throughout a wide area in the central portion of northeastern Brazil, including parts of the states of Maranhão, Piauí, Tocantins, Pará, Ceará and Goiás. It has a total area of 600,000 km2 and its depocenter contains a 500 m thick sedimentary succession of Mesozoic rocks (Campbell 1949Campbell D.F. 1949. Revised report on the reconnaissance geology of the Maranhão Basin. Relatório Interno. Rio de Janeiro, Conselho Nacional do Petróleo, 117 p., Mesner & Wooldridge 1964aMesner J.C., & Wooldridge L.C.P. 1964a. Estratigrafia das bacias paleozoicas e cretáceas do Maranhão. Boletim Técnico Petrobras, 7(2):137-164.).

The Codó Formation is the richest fossiliferous unit in the Parnaíba Basin and is distributed over an area of approximately 170,000 km2 (Lisboa 1914Lisboa M.A.R. 1914. The Permian geology of Northern Brazil. American Journal of Science, 37:425-443. DOI: 10.2475/ajs.s4-37.221.425
https://doi.org/10.2475/ajs.s4-37.221.42...
, Lima 1982Lima M.R. 1982. Palinologia da Formação Codó na região de Codó. Boletim Instituto de Geociências da USP, 13:116-128.). In the last decade, several specimens have been described for this unit, including crustaceans (isopods), mollusks (gastropods and bivalve), fishes, and plants (Lindoso 2016Lindoso R.M. 2016. A biota da Formação Codó (Aptiano da Bacia do Parnaíba), Nordeste do Brasil: aspectos paleoambientais e paleobiogeográficos. PhD Thesis, Instituto de Geologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Rio de Janeiro, 161 p., Lindoso & Carvalho 2012Lindoso R.M., & Carvalho I. 2012. Crustáceos da Formação Codó (Bacia do Parnaíba, Brasil. In: Lopes F.C., Andrade A.I., Henriques M.H., Quinta-Ferreira M., Barata M.T., Pena dos Reis R. (eds.). Para entender a Terra: memórias e notícias de geociências no espaço lusófono. Portugal, Imprensa da Universidade de Coimbra, cap. 17, p. 171-177., Lindoso et al. 2011Lindoso R.M., Carvalho I.S., Medeiros M.A., Pereira A.A., Santos R.A.B., Mendes I.D., Brito J.M., Bôas I.V., Araújo M.N., Ferreira N.N. 2011. Novos sítios fossilíferos em carbonatos da Formação Codó (Aptiano-Albiano) da Bacia do Parnaíba, Maranhão, Brasil In: Carvalho I.S., Srivastava N.K., Strohschoen Jr. O.S., Lana C.C. (eds.). Paleontologia: Cenários de Vida. Rio de Janeiro, Interciência , p. 819-827., 2013aLindoso R.M., Carvalho I.S., Medeiros M.A., Mendes I.D., Marques N.E., Brito R., Almeida C.M. 2013a. A megaflora da Formação Codó (Aptiano, Bacia do Parnaíba), nordeste do Brasil. In: 23º Congresso Brasileiro de Paleontologia, 23., Gramado. Annals... Gramado, SBP, p. 175-176., 2013bLindoso R.M., Carvalho I.S., Mendes I.D. 2013b. An isopod from the Codó Formation (Aptian of the Parnaíba Basin), Northeastern Brazil. Brazilian Journal of Geology, 43(1):16-21. DOI: 10.5327/Z2317-48892013000100003
https://doi.org/10.5327/Z2317-4889201300...
, 2016Lindoso R.M., Maisey J.G., Carvalho I.S. 2016. Ichthyofauna from the Codó Formation, Lower Cretaceous (Aptian, Parnaíba Basin), Northeastern Brazil and their paleobiogeographical and paleoecological significance. Palaeogeography, Palaeoclimatology, Palaeoecology, 447:53-64. DOI: 10.1016/j.palaeo.2016.01.045
https://doi.org/10.1016/j.palaeo.2016.01...
, Brito et al. 2016Brito P.M., Lindoso R.M., Carvalho I.S., Machado G.P. 2016. Discovery of Obaichthyidae gars (Holostei, Ginglymodi, Lepisosteiformes) in the Aptian Codó Formation of the Parnaíba Basin: remarks on paleobiogeographical and temporal range. Cretaceous Research, 59:10-17. https://doi.org/10.1016/j.cretres.2015.10.017
https://doi.org/10.1016/j.cretres.2015.1...
). Its fossil record in the central-north part of Maranhão State is characterized by a discontinuous occurrence over a wide area, cropping out mainly in the cliffs of the river valleys that drain the central part of the basin (Santos & Carvalho 2009Santos M.E.C.M., & Carvalho M.S.S. 2009. Paleontologia das bacias Parnaíba, Grajaú e São Luís. Rio de Janeiro, CPRM, 215 p.). The fplant fossils herein described come from near the margins of the Parnaiba river, in Brejo County (Fig. 2).

Figure 2:
A stratigraphic profile of the Faveirinha Quarry (A) and Perneta Ranch (B), in Brejo City, Maranhão. In (C) and (D) the same outcrops expose the levels of the Codó Formation containing plant fossils.

The geology of the Codó Formation was initially reported by Lisboa (1914Lisboa M.A.R. 1914. The Permian geology of Northern Brazil. American Journal of Science, 37:425-443. DOI: 10.2475/ajs.s4-37.221.425
https://doi.org/10.2475/ajs.s4-37.221.42...
). Later, Campbell (1949Campbell D.F. 1949. Revised report on the reconnaissance geology of the Maranhão Basin. Relatório Interno. Rio de Janeiro, Conselho Nacional do Petróleo, 117 p.), also classified this unit as bituminous shales associated with limestone and gypsum lenses identified at the Itapecuru river valley, in Codó County. It was then further confirmed by Assine (1992Assine M.L. 1992. Análise estratigráfica da Bacia do Araripe, Nordeste do Brasil. Revista Brasileira de Geociências, 22:289-300.). Additionally, siltstone, sandstone and evaporite levels were also described for the Codó Formation (Vaz et al. 2007Vaz P.T., Rezende N.G.A.M., Filho J.R.W., Travassos W.A.S. 2007. Bacia do Paraíba. Boletim de Geociências Petrobras, 15:253-263.). Although an Aptian/Albian age was previously suggested for this unit based on palynology (Lima 1982Lima M.R. 1982. Palinologia da Formação Codó na região de Codó. Boletim Instituto de Geociências da USP, 13:116-128.), it was later restricted to the Aptian, based on the lower limit of the overlying unit (Itapecuru Formation), considered upper Aptian in age (Pedrão et al. 1996Pedrão E., Barrilari I.M.R., Lima H.P. 1996. Palynological studies in the Cretaceous of the Parnaíba basin. In: Congresso Brasileiro de Geologia, 39. Annals… Salvador, Sociedade Brasileira de Geologia, p. 380-383.).

The palynological data analyzed by Lima and Leite (1978Lima E.A.A., & Leite J.F. 1978. Projeto de estudo global dos recursos minerais da bacia sedimentar do Parnaíba: integração geológico-metalogenética. Relatório Final, Etapa III. Recife, DNPM-CPRM, 16 v., 473 p.) indicate marine to brackish lacustrine environments in the Codó Formation. Later, it was confirmed by a facies analysis presented by Rossetti et al. (2001Rossetti D.F., Góes A.M., Arai M. 2001. A passagem Aptiano-Albiano na Bacia do Grajaú. In: Rossetti D.F., Góes A.M., Truckenbrodt W. (eds.). O Cretáceo na Bacia de São Luís-Grajaú. Belém, Museu Paraense Emílio Goeldi, Coleção Friedrich Katzer, p. 101-117.). With regard to the inferred lagoon context, three distinct phases were established, evolving in time from central lake to marginal marine environments, influenced by arid to semiarid climate conditions. The marine fossils, recorded at both Parnaíba and São Luís basins, occur in the upper levels of the Codó Formation and they contain fossil plants.

Fish remains (Silva-Santos 1985Silva-Santos R. 1985. Paleoictiofauna da Formação Codó, Bacia do Parnaíba, NE do Brasil. In: Congresso Brasileiro de Paleontologia, 9, Fortaleza, Brasil. Resumos, p. 11., Lindoso et al. 2016Lindoso R.M., Maisey J.G., Carvalho I.S. 2016. Ichthyofauna from the Codó Formation, Lower Cretaceous (Aptian, Parnaíba Basin), Northeastern Brazil and their paleobiogeographical and paleoecological significance. Palaeogeography, Palaeoclimatology, Palaeoecology, 447:53-64. DOI: 10.1016/j.palaeo.2016.01.045
https://doi.org/10.1016/j.palaeo.2016.01...
), dinoflagellates (Antonioli 2001Antonioli L. 2001. Estudo palino-cronoestratigráfico da Formação Codó - Cretáceo Inferior do Nordeste Brasileiro. Thesis. Instituto de Geologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, 265 p.), and isopod crustaceans (Lindoso et al. 2013bLindoso R.M., Carvalho I.S., Mendes I.D. 2013b. An isopod from the Codó Formation (Aptian of the Parnaíba Basin), Northeastern Brazil. Brazilian Journal of Geology, 43(1):16-21. DOI: 10.5327/Z2317-48892013000100003
https://doi.org/10.5327/Z2317-4889201300...
) support the sea-level rise at the end of Aptian (Weissert et al. 1998Weissert H., Lini A., Föllmi K.B., Kuhn O. 1998. Correlation of Early Cretaceous carbon isotope stratigraphy and platform drowning events: a possible link? Palaeogeography, Palaeoclimatology, Palaeoecology, 137:189-203. DOI: 10.1016/S0031-0182(97)00109-0
https://doi.org/10.1016/S0031-0182(97)00...
), and in many other coastal basins from Northeast Brazil. According to Arai (2014Arai M. 2014. Aptian/Albian (Early Cretaceous) paleogeography of the South Atlantic: a paleontological perspective. Brazilian Journal of Geology, 44(2):339-350. DOI: 10.5327/Z2317-4889201400020012
https://doi.org/10.5327/Z2317-4889201400...
) and Lindoso et al. (2016Lindoso R.M., Maisey J.G., Carvalho I.S. 2016. Ichthyofauna from the Codó Formation, Lower Cretaceous (Aptian, Parnaíba Basin), Northeastern Brazil and their paleobiogeographical and paleoecological significance. Palaeogeography, Palaeoclimatology, Palaeoecology, 447:53-64. DOI: 10.1016/j.palaeo.2016.01.045
https://doi.org/10.1016/j.palaeo.2016.01...
), the invasion of seawater at that time must have originated from the north and through the Central/Equatorial Atlantic or Eastern Tethys.

The palyno-chronostratigraphic proposal of Antonioli (2001Antonioli L. 2001. Estudo palino-cronoestratigráfico da Formação Codó - Cretáceo Inferior do Nordeste Brasileiro. Thesis. Instituto de Geologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, 265 p.) also divided the Codó Formation into three lithostratigraphic intervals and confirmed that each had the highest influence in open marine conditions along the deposition, with a medium interval characterized by essentially evaporitic deposits. The plant fossils beds are part of the upper interval, which has been interpreted to be an upper shoreface environment, with an interdistributary lagoon/bay, suspension lobes and distributary channels (Paz & Rossetti 2001Paz J.D., & Rossetti D.F. 2001. Reconstrução paleoambiental da Formação Codó (Aptiano), borda leste da Bacia do Grajaú, MA. In: Rossetti D.F., Góes A.M., Truckenbrodt W. (eds.). O Cretáceo Na Bacia de São Luís-Grajaú. Belém, Museu Paraense Emílio Goeldi, Coleção Friedrich Katzer, p. 77-100., Rossetti et al. 2001Rossetti D.F., Góes A.M., Arai M. 2001. A passagem Aptiano-Albiano na Bacia do Grajaú. In: Rossetti D.F., Góes A.M., Truckenbrodt W. (eds.). O Cretáceo na Bacia de São Luís-Grajaú. Belém, Museu Paraense Emílio Goeldi, Coleção Friedrich Katzer, p. 101-117.).

The fossil plants herein described were collected in the Faveirinha (42º44’45.4”W/ 03º49’20.1”S) and Perneta Ranch quarries (42º44’21.1”W/ 03º48’50.0”S), nearly 20 km from Brejo County (Fig. 2). They were collected in massive and fine laminated limestone and interbedded with marls and calcareous concretions, which compose the upper levels of the Codó Formation (Fig. 2A and 2B).

MATERIAL AND METHODS

The plant fossils impressions in the Codó Formation beds, which diversity are represented by few specimens, allows detecting eleven distinct types of branches and leaves linked to gymnosperms and angiosperms. Those related to conifers and Gnetales were compare with others Early Cretaceous previously known morphogenera, and the angiosperm treated by the informal system introduced by Hickey (1973Hickey L.J. 1973. Classification of the architecture of dicotyledoneous leaves. American Journal of Botany, 60:17-33.), Hickey and Wolf (1975Hickey L.J., & Wolfe J.A. 1975. The bases of angiosperm phylogeny: vegetative morphology. Annals of the Missouri Botanical Garden, 62:538-589. https://doi.org/10.2307/2395267
https://doi.org/10.2307/2395267...
), and more recently stablished by Ellis et al. (2009Ellis B., Daly D., Hickey L.J., Johnson K.R., Mitchell J., Wilf P., Wing S.L. 2009. Manual of Leaf Architecture. Ithaca, Cornell University Press, 190 p.). The leaf architecture and venation patterns of the flowering plants were described considering the new taxonomic rules (McNeill et al. 2012McNeill J., Barrie F.R., Buck W.R., Demoulin V., Greuter W., Hawksworth D.L., Herendeen P.S., Knapp S., Marhold K., Prado W.F., Van Reine P.H., Smith G.F., Wiersema J.H. 2012. International Code of Nomenclature for algae, fungi, and plants (Melbourne Code): adopted by the Eighteenth International Botanical Congress Melbourne, Australia, July 2011. Regnum Vegetabile 154. Australia, Koeltz Scientific Books.) and treated by morphotypes or fossil taxa. Affinities with previously described fossils were proposed, looking for correlations with other preserved assemblages from tropical Cretaceous basins.

Concerning the flowering plants, a code name was used, which follows the procedure applied today in angiosperm fossil materials from levels that precede the Early Miocene (e.g., Pole 1993Pole M.S. 1993. Early Miocene flora of the Manuherikia Group, New Zealand, 8. Nothofagus. Journal of the Royal Society of New Zealand, 23(4):329-344. https://doi.org/10.1080/03036758.1993.10721230
https://doi.org/10.1080/03036758.1993.10...
, Iglesias et al. 2007Iglesias A., Zamuner A.B., Poiré D.G., Larriestra F. 2007. Diversity, taphonomy and palaeoecology of an angiosperm flora from the Cretaceous (Cenomanian-Coniacian) in Southern Patagonia, Argentina. Palaeontology, 50(2):445-466. DOI: 10.1111/j.1475-4983.2007.00639.x
https://doi.org/10.1111/j.1475-4983.2007...
). Here, two initial letters - CF, referring to Codó Formation - and numbers, separate the different morphotypes.

Analyses and illustrations of the fossil material were made using an Olympus SZH Stereomicroscope with a camera lucida. Photographs were taken using a Fujifilm Finepix HS50exr digital camera system. To enhance the contrast and highlight the fine details, a record in low-angle light and close-up lens were used. The described samples are housed in the paleontological collection of the Department of Geology at the Universidade Federal do Rio de Janeiro (UFRJ), Brazil, under the following numbers: (UFRJ-DG 1988-Pb, UFRJ-DG 1987-Pb, UFRJ-DG 1944-Pb, UFRJ-DG 1984-Pb, UFRJ-DG 1457-Pb, UFRJ-DG 1986-Pb, UFRJ-DG 1983-Pb, UFRJ-DG 1985-Pb, UFRJ-DG 1800-Pb, UFRJ-DG 1999-Pb, UFRJ-DG 1990-Pb).

DESCRIPTION OF THE FOSSIL PLANTS AND THEIR CORRELATIONS

Gymnosperms Order GNETALES Luerss 1869 cf. Drewria potomacensis Crane et Upchurch Jr., 1987Crane P.R., & Upchurch Jr. G.R. 1987. Drewria potomacensis gen. et. sp. nov., an Early Cretaceous member of Gnetales from the Potomac Group of Virginia. American Journal of Botany, 74:1722-1736. ( Fig. 3A-C )

Material

UFRJ-DG1444-Pb, a cast of a vegetative branch and its associated leaves.

Description

An axillary striate and monopodial vegetative branch with a slender stem (2 mm width) and two lateral branches (1 mm width), one time irregularly forked and planar disposed. Leaves simple, opposite and oblong in form, with entire margins, acute apices, and decurrent bases, diverging from a swollen node. The proximal ones (30 mm long, 4 mm wide on average) have sheathing bases (Fig. 3A-B). The central axis (0.5 mm wide) bear leaves with an apparently highlighted mid vein or vascular bundle, laterally accompanied by parallel veins (Fig. 3C). Weak and rare transverse connections apically oriented (chevrons?) were preserve in a single sector (Fig. 3B).

Figure 3:
Gnetales (A,B,C) and conifer-related forms (D,E,F) in the Codó Formation flora. (A) Monopodial and trifurcate dichotomous branch, one time irregularly forked, carrying opposite, oblong leaves, comparable to those associate of the reproductive structure of Drewria potomacencis Crane and Upchurch (UFRJ-DG1444-Pb); (B) outline of the shoot in A, showing the fine details of venation with probable apically orientated chevrons (arrow); (C) detail of the axillary branch venation; (D) Cupressinocladus sp. (UFRJ-DG1987-Pb), branch impression with sub-opposite spreading bifacial, cushion-like and keeled leaves; (E) cf. Brachyphyllum sp. (UFRJ-DG1988-Pb), impression of an apical branch and of the sub-alternate to opposite second order branches; (F) detail of E, highlighting the apical contours of the spirally disposed leaves and their radial striations. Figures 3C and 3F are detailed reproductions of the figures 3A and 3E, respectively. Scale bars: 1 cm.

Remarks

The set of morphological features, as the trifurcate dichotomous branching pattern, striate planar leaf axes, linear elongated sheathing and oblong multi-veined leaves with opposite (decussate?) arrangement, associate to high-order cross veins preserving rare anastomoses in chevrons, approximate this morphotype to those found in previous described gnetophytes (Kunzmann et al. 2009Kunzmann L., Mohr B.A.R., Bernardes-de-Oliveira M.E.C. 2009. Cearania heterophylla gen. nov. et sp. nov., a fossil gymnosperm with affinities to the Gnetales from the Early Cretaceous of northern Gondwana. Review of Palaeobotany and Palynology, 158:193-212. DOI: 10.1016/j.revpalbo.2009.09.001
https://doi.org/10.1016/j.revpalbo.2009....
, 2011Kunzmann L., Mohr B.A.R., Wilde V., Bernardes-de-Oliveira M.E.C. 2011. A putative gnetalean gymnosperm Cariria orbiculiconiformis gen. nov. et spec. nov. from the Early Cretaceous of northern Gondwana. Review of Palaeobotany and Palynology, 165:75-95. DOI: 10.1016/j.revpalbo.2011.02.005
https://doi.org/10.1016/j.revpalbo.2011....
, Seward 2010Seward A.C. 2010. Fossil Plants: A Text-Book for students of botany and geology: Ginkgoales, Coniferales, Gnetales. New York, Cambridge University Press , v. 5, 545 p., Ricardi-Branco et al. 2013Ricardi-Branco F., Torres M., Tavares S.S., Carvalho I.S., Tavares P.G.E., Campos A.C.A. 2013. Itajuba yansanae gen, and sp. nov. of Gnetales, Araripe Basin (Albian-Aptian) in Northeast Brazil. In: Zhang Y., Ray P. (eds.). Climate change and regional/local responses, chapter 7, p. 187-205. DOI: 10.5772/55704
https://doi.org/10.5772/55704...
). Among the known fossils, such morphological features characterize Drewria potomacensisCrane (Crane & Upchurch Jr., 1987Crane P.R., & Upchurch Jr. G.R. 1987. Drewria potomacensis gen. et. sp. nov., an Early Cretaceous member of Gnetales from the Potomac Group of Virginia. American Journal of Botany, 74:1722-1736.), described by Doyle and Hickey (1976Doyle J.A., & Hickey L.J. 1976. Pollen and leaves from the Mid-Cretaceous Potomac group and their bearing on early angiosperm evolution. In: Beck C.B. (ed.). Origin and early evolution of angiosperms. New York, Columbia University Press, p. 139-206.) to the Zone I Potomac Group. Nevertheless, the Codó branch exhibits some distinct features, like more elongated leaves that are not so clearly decussated in the arrangement, and a slight prominent strand or mid-rib. Its origin, however, in the branch axis suggests that more than a vein could represent a concentrated bundle of fibers. On the other hand, the convergence of the main veins in the apices of the leaves in the herein described fossil (Fig. 3B) is similar to that mentioned by Crane and Upchurch Jr. (1987Crane P.R., & Upchurch Jr. G.R. 1987. Drewria potomacensis gen. et. sp. nov., an Early Cretaceous member of Gnetales from the Potomac Group of Virginia. American Journal of Botany, 74:1722-1736.) to Welwitschia and Drewria.

According to Gandolfo et al. (2000Gandolfo M.A., Nixon K.C., Crepet W. 2000. Monocotyledons: a review of their Cretaceous record. In: Wilson K.L., Morrison D.A. (eds.). Monocots: systematics and evolution. Australia, Csiro, p. 44-51.), the presence of a midvein in some elongated leaves is not a definitive criterion to discard the Gnetales from possible affinities, since modern Gnetum have a well-developed main vein. Moreover, similar morphologies to that of Drewria, including “chevrons”, characterize Welwitschia and the even now dubious Early Cretaceous monocot Acaceaephyllum Fontaine. However, the latter, like Gnetum, has a pinnate venation (Sender et al. 2012Sender L.M., Villanueva-Amadoz U., Diez J.B., Sanchez-Pellicer R., Bercovici A., Pons D., Ferrer J. 2012. A new uppermost Albian flora from Teruel province, northeastern Spain. Geodiversitas, 34(2):373-397. DOI: 10.5252/g2012n2a7
https://doi.org/10.5252/g2012n2a7...
).

With other gnetalean from Lower Cretaceous of Brazil, the Codó branch only shares the longitudinally striated axes, here without visible nodes. The preserved specimens, Itajuba yansanae, Cearania heterophylla, and Cariria orbiculiconiformis, differ in sympodial axes and have round and short leaves, or are represented by reproductive structures and woods (Kunzmann et al. 2009Kunzmann L., Mohr B.A.R., Bernardes-de-Oliveira M.E.C. 2009. Cearania heterophylla gen. nov. et sp. nov., a fossil gymnosperm with affinities to the Gnetales from the Early Cretaceous of northern Gondwana. Review of Palaeobotany and Palynology, 158:193-212. DOI: 10.1016/j.revpalbo.2009.09.001
https://doi.org/10.1016/j.revpalbo.2009....
, 2011Kunzmann L., Mohr B.A.R., Wilde V., Bernardes-de-Oliveira M.E.C. 2011. A putative gnetalean gymnosperm Cariria orbiculiconiformis gen. nov. et spec. nov. from the Early Cretaceous of northern Gondwana. Review of Palaeobotany and Palynology, 165:75-95. DOI: 10.1016/j.revpalbo.2011.02.005
https://doi.org/10.1016/j.revpalbo.2011....
, Ricardi-Branco et al. 2013Ricardi-Branco F., Torres M., Tavares S.S., Carvalho I.S., Tavares P.G.E., Campos A.C.A. 2013. Itajuba yansanae gen, and sp. nov. of Gnetales, Araripe Basin (Albian-Aptian) in Northeast Brazil. In: Zhang Y., Ray P. (eds.). Climate change and regional/local responses, chapter 7, p. 187-205. DOI: 10.5772/55704
https://doi.org/10.5772/55704...
). As such, it is impossible to compare them with the vegetative branch herein described.

As previously observed, the Gnetales are an important component in the palynological assemblage of the Codó Formation, the Santana Formation (Portela et al. 2014Portela H.A., Antonioli L., Dino R., Garcia M.J. 2014. Caracterização palinoflorística e paleoambiental da Formação santana (Cretáceo Inferior), poço 4-bo-1-pe, Bacia do Araripe, nordeste do Brasil. Revista Brasileira de Paleontologia, 17(3):363-372. DOI: 10.4072/rbp.2014.3.07
https://doi.org/10.4072/rbp.2014.3.07...
) and the basal Potomac Group (Doyle & Hickey 1976Doyle J.A., & Hickey L.J. 1976. Pollen and leaves from the Mid-Cretaceous Potomac group and their bearing on early angiosperm evolution. In: Beck C.B. (ed.). Origin and early evolution of angiosperms. New York, Columbia University Press, p. 139-206.). For Crane and Upchurch Jr. (1987Crane P.R., & Upchurch Jr. G.R. 1987. Drewria potomacensis gen. et. sp. nov., an Early Cretaceous member of Gnetales from the Potomac Group of Virginia. American Journal of Botany, 74:1722-1736.), the absence of extensive secondary tissues in the Gnetales and in Drewria, indicates that it is an herbaceous plant.

Recently, Yang et al. (2015Yang Y., Lin L., Ferguson D.K. 2015. Parallel evolution of leaf morphology in gnetophytes. Organisms, Diversity & Evolution, 15:651-662. DOI: 10.1007/s13127-015-0226-6
https://doi.org/10.1007/s13127-015-0226-...
) proposed that the decussate phyllotaxy in the reproductive shoots of D. potomacencis, and its leaf morphology, similar to that of Ephedra multinervis from China, guarantees that Drewria and other Gnetales are in an intermediate phylogenetic position, between Ephedrales and Welwitschiales.

Order CONIFERALES sensu Farjon, 2010 ?Family Cheirolepidiaceae Tahktajan, 1963 Cupressinocladus Seward, 1919Seward A.C. 1919. Fossil Plants. Cambridge, Cambridge University Press, v. 4, 543 p. ( Fig. 3D )

Material

UFRJ-DG1987-Pb, part of an ultimate shoot.

Description

Erect and short, one-branched, leafy stem (c. 30 mm long, 6-7 mm wide). Leaves bifacially disposed, cushion-like and keeled (5-3 mm long, 3-2 mm wide), rhomboidal in transverse section, with fleshy to leathery texture apparently opposite to sub-opposite (helically?) arranged. The broad basal part of the leaves is sessile attached to the axis and the middle and distal ones are free. Apex varies between acute-obtuse to slightly falcate. Venation indistinct and margins apparently irregular.

Remarks

Leafy branches with decussate to slightly helically arranged leaves, longer than wide, with a broad basal cushion and free apices, characterize the extant Cupressaceae. In the fossil record, they are generally related to the morph genera CupressinocladusSeward (link to the Cupressaceae by Seward 1919Seward A.C. 1919. Fossil Plants. Cambridge, Cambridge University Press, v. 4, 543 p.) or to Pagiophyllum Heer (sensuStewart & Rothwell 1993Stewart W.N., & Rothwell G.W. 1993. Paleobotany and the evolution of plants. 2ª ed. United Kingdom, Cambridge University Press, 525 p., fig. 29.7B). Among them, the homogeneous round to rhomboidal leaves of Cupressinocladus, flattened and oppositely disposed along the shoot, are closer to the morphotype herein described. In general, when including in the Cheirolepidiaceae, some researchers prefer to maintain its affinities unresolved (Pons 1988Pons D. 1988. Le Mésozoique de Colombie: macroflores et microflores. Paris, Cahier Micropaleontologie, CNRS, 168 p. , Pole 2000Pole M.S. 2000. Mid-Cretaceous Conifers from the Eromanga Basin, Australia. Australian Systematic Botany, 13:153-197. https://doi.org/10.1071/SB99001
https://doi.org/10.1071/SB99001...
, Van Waveren et al. 2002Van Waveren I.M., van Konijnenburg-van Cittert J.H.A., van der Burgh J., Dilcher D.L. 2002. Macrofloral remains from the Lower Cretaceous of the Leiva region (Colombia). Scripta Geologica, 123:1-39., Gee 2010Gee C. (ed.). 2010. Plants in Mesozoic Time: morphological innovations, phylogeny, ecosystems. Indiana: Indiana University Press, 374 p.).

Related shoot morphologies is until now rare in the Cretaceous assemblages of northeastern Brazil, the only exception being an isolated shoot that is still undescribed from the Riachuelo Formation (Aptian-Albian), Sergipe-Alagoas basin (Dutra et al. 2002Dutra T.L., Boardman D.R., Souza-Lima W. 2002. Os fósseis da bacia de Sergipe-Alagoas. Plantas: Gimnospermas. Phoenix, 46:1-4.), and in some decurrent leaves of the heterophilic shoots of Tomaxelia Archangelsky, identified in Santana Formation, Araripe Basin by Kunzmann et al. (2006Kunzmann L., Mohr B., Bernardes-de-Oliveira M.E.C., Wilde V. 2006. Gymnosperms from the Lower Cretaceous Crato Formation (Brazil). II. Cheirolepidiaceae. Fossil Record, 9:213-225. DOI: 10.1002/mmng.200600009
https://doi.org/10.1002/mmng.200600009...
), and included in the Cheirolepidiaceae. However, Tomaxelia has helically arranged leaves, a distinct phyllotaxy to that of the branch herein preserved.

“Cupressoid” foliages are, however, common in other Equatorial areas of South America (Zijlstra & Kvaček, 2010Zijlstra G., & Kvaček Z. 2010. (1924) Proposal to conserve the name Cupressinocladus against Libocedrites (fossil Coniferophyta). Taxon, 59(1):301. DOI: 10.2307/27757081
https://doi.org/10.2307/27757081...
), especially in the levels of the Paja Formation, in Colombia, where seven distinct species assigned to Cupressinocladus were recorded (Pons 1988Pons D. 1988. Le Mésozoique de Colombie: macroflores et microflores. Paris, Cahier Micropaleontologie, CNRS, 168 p. , Van Waveren et al. 2002Van Waveren I.M., van Konijnenburg-van Cittert J.H.A., van der Burgh J., Dilcher D.L. 2002. Macrofloral remains from the Lower Cretaceous of the Leiva region (Colombia). Scripta Geologica, 123:1-39., Plate 4, Fig. 1; Sucerquia 2013Sucerquia P.A. 2013. Taxonomia, modos de preservação e fitogeografia de coníferas aptianas da região paleoequatorial da América do Sul. PhD Thesis, Instituto de Geociências da Universidade de São Paulo, São Paulo, 86 p., 13 pranchas.), and included in the Cheirolepidiceae (Meyen 1987Meyen S.V. 1987. Fundamentals of Paleobotany. New York, Chapman & Hall, 431p., Taylor et al. 2009Taylor T.N., Taylor E.L., Krings M. 2009. Paleobotany: The Biology and Evolution of Fossil Plants. Burlington/London/San Diego/New York, Elsevier/Academic Press Inc., 1,230 p.). First detected in Gondwana assemblages, their older lineages (Berriasian-Barremian) came from southern Eurasia (Kimura et al. 1992Kimura T., Ohana T., Naito G. 1992. Cupressinocladus sp., newly found from the Lower Cretaceous Wakino Formation, West Japan. Bulletin of the Kitakyushu Museum of Natural History, 11:79-86., Coiffard et al. 2007Coiffard C., Gomez B., Thevenard F. 2007. Early Cretaceous Angiosperm invasion of Western Europe and Major Environmental Changes. Annals of Botany, 100:545-553. DOI: 10.1093/aob/mcm160
https://doi.org/10.1093/aob/mcm160...
), where Cupressinocladus is commonly registered with Brachyphyllum and Frenelopsis/Pseudofrenelopsis.

Younger similar planar shoots and cushion-like leaves were found in other putative Cheirolepidiaceae of North America (Glen Rose Formation, Texas), like Glenrosa (Watson & Fisher 1984Watson J., & Fisher H.L. 1984. A new conifer genus from the Lower Cretaceous Glen Rose Formation, Texas. Palaeontology, 27:719-727. emend. Srinivasan 1992Srinivasan V. 1992. Two new species of the conifer Glenrosa from the Lower Cretaceous of North America. Review of Palaeobotany and Palynology, 72:245-255. https://doi.org/10.1016/0034-6667(92)90029-G
https://doi.org/10.1016/0034-6667(92)900...
), which is characterized by keeled leaves with free acute-obtuse apices and fringed margins (e.g., G. falcataGomez, Gomez et al. 2012Gomez B, Ewin T.A.M., Daviero-Gomez V. 2012. The conifer Glenrosa falcata sp. nov. from the Lower Cretaceous of Spain and its palaeoecology. Review of Palaeobotany and Palynology, 172:21-32. DOI: 10.1016/j.revpalbo.2012.01.009
https://doi.org/10.1016/j.revpalbo.2012....
). It has a broad temporal (Barremian to Cenomanian) and paleogeographic distribution in tropical areas and has been found to be associated to hypersaline lagoons and bay deposits (Srinivasan 1995Srinivasan V. 1995. Conifers from the Puddledock locality (Potomac Group, Early Cretaceous) in eastern North America. Review of Palaeobotany and Palynology, 89:257-286. DOI: 10.1016/0034-6667(95)00010-8
https://doi.org/10.1016/0034-6667(95)000...
, Zhou et al. 2000Zhou Z., Thévénard F., Barale G., Guignard G. 2000. A new xeromorphic conifer from the Cretaceous of East China. Palaeontology, 43(3):561-572. DOI: 10.1111/j.0031-0239.2000.00140.x
https://doi.org/10.1111/j.0031-0239.2000...
, Gomez et al. 2012Gomez B, Ewin T.A.M., Daviero-Gomez V. 2012. The conifer Glenrosa falcata sp. nov. from the Lower Cretaceous of Spain and its palaeoecology. Review of Palaeobotany and Palynology, 172:21-32. DOI: 10.1016/j.revpalbo.2012.01.009
https://doi.org/10.1016/j.revpalbo.2012....
, Moreau et al. 2015Moreau J.-D., Néraudeau D., Tafforeau P., Dépré É. 2015. Study of the histology of leafy axes and male cones of Glenrosa carentonensis sp. nov. (Cenomanian Flints of Charente-Maritime, France), using synchrotron microtomography linked with palaeoecology. PLoS One, 10(8):e0134515. DOI: 10.1371/journal.pone.0134515
https://doi.org/10.1371/journal.pone.013...
). In the coastal marine environments of the Potomac beds, it occurs along with other xerophytic Cheirolepidiceae (Watson & Fischer 1984Watson J., & Fisher H.L. 1984. A new conifer genus from the Lower Cretaceous Glen Rose Formation, Texas. Palaeontology, 27:719-727., Srinivasan 1995Srinivasan V. 1995. Conifers from the Puddledock locality (Potomac Group, Early Cretaceous) in eastern North America. Review of Palaeobotany and Palynology, 89:257-286. DOI: 10.1016/0034-6667(95)00010-8
https://doi.org/10.1016/0034-6667(95)000...
, Zhou et al. 2000Zhou Z., Thévénard F., Barale G., Guignard G. 2000. A new xeromorphic conifer from the Cretaceous of East China. Palaeontology, 43(3):561-572. DOI: 10.1111/j.0031-0239.2000.00140.x
https://doi.org/10.1111/j.0031-0239.2000...
, Tanrikulu et al. 2015Tanrikulu S., Doyle J., Delusina I. 2015. Pollen and spores of the Glen Rose Formation (Early Albian, Texas) and their implications for correlation of other sequences. GSA Annual Meeting in Baltimore, Maryland, (17-14).), in paleoenvironmental conditions similar to those of the from Santana and Codó Formations deposits (Antonioli 2001Antonioli L. 2001. Estudo palino-cronoestratigráfico da Formação Codó - Cretáceo Inferior do Nordeste Brasileiro. Thesis. Instituto de Geologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, 265 p.).

Also, SeditesGeinitz, from the German Cretaceous (upper Turonian “Plänerkalk” horizon of Geinitz 1842Geinitz H.B. 1842. Charakteristik der Schichten und Petrefacten des sächsisch-böhmischen Kreidegebirges, 3. Heft: Die sächsisch-böhmische Schweiz, die Oberlausitz und das Innere von Böhmen, Index Petrefactarum. Dresden, Arnoldische Buchhandlung, 120 p.), shares the spread disposed leaves in apparent four rows of opposite decussate pairs (Kunzmann 2010Kunzmann L. 2010. Geinitzia reichenbachii (Geinitz, 1842) Hollick and Jeffrey, 1909 and Sedites rabenhorstii Geinitz, 1842 (Pinopsida; Late Cretaceous) reconsidered and redescribed. Review of Palaeobotany and Palynology, 159:123-140. DOI: 10.1016/j.revpalbo.2009.11.006
https://doi.org/10.1016/j.revpalbo.2009....
). In S. rabenhorstii Geinitz, opposite pairs of leaves with decurrent bases (35 mm long) are arranged along an unbranched terminal shoot and are represented by scarce materials. Kunzmann (2010Kunzmann L. 2010. Geinitzia reichenbachii (Geinitz, 1842) Hollick and Jeffrey, 1909 and Sedites rabenhorstii Geinitz, 1842 (Pinopsida; Late Cretaceous) reconsidered and redescribed. Review of Palaeobotany and Palynology, 159:123-140. DOI: 10.1016/j.revpalbo.2009.11.006
https://doi.org/10.1016/j.revpalbo.2009....
) associated it with a dubious Cheirolepidiaceae.

The apical shoot herein associated to Cupressinocladus differs, however, from two other Cretaceous conifers of low latitudes, carrying decussate disposed leaves, Geinitzia and Frenelopsis. Geinitzia Endl. has bilateral and more elongated leaves which are helically disposed (Stewart & Rothwell 1993Stewart W.N., & Rothwell G.W. 1993. Paleobotany and the evolution of plants. 2ª ed. United Kingdom, Cambridge University Press, 525 p.). Frenelopsis Schenk emend. Watson, has slender spreading leaves that are disposed in whorls (Barale & Ouaja 2002Barale G., & Ouaja M. 2002. La biodiversité végétale des gisements d’age Jurassique supérieure -Crétacé inférieur de Merbah El Asfer (Sud-Tunisien). Cretaceous Research, 23:707-737., Gomez et al. 2002Gomez B., Martín-Closas C., Barale G., de Porta N.S., Thévenard F., Guignard F. 2002. Frenelopsis (Coniferales: Cheirolepidiacea) and related male organ genera from the Lower Cretaceous of Spain. Palaeontology, 45(5):997-1036. DOI: 10.1111/1475-4983.00273
https://doi.org/10.1111/1475-4983.00273...
, Kunzmann et al. 2006Kunzmann L., Mohr B., Bernardes-de-Oliveira M.E.C., Wilde V. 2006. Gymnosperms from the Lower Cretaceous Crato Formation (Brazil). II. Cheirolepidiaceae. Fossil Record, 9:213-225. DOI: 10.1002/mmng.200600009
https://doi.org/10.1002/mmng.200600009...
, Burger & Ward 2016Burger B.J., & Ward C.J. 2016. On the occurrence of fossil conifers with affinities to Geinitzia in the late Cretaceous (Campanian) Mesaverde Group, Williams Fork Formation of northeastern Utah, U.S.A. PeerJ Preprints, 4:e1862v1. DOI: 10.7287/peerj.preprints.1862v1
https://doi.org/10.7287/peerj.preprints....
).

In a more recent study, Arens and Allens (2014Arens N.C., & Allen S.E. 2014. A florule from the base of the Hell Creek Formation in the type area of eastern Montana: implications for vegetation and climate. In: Wilson G.P., Clemens W.A., Horner J.R., Hartman J.H. (eds.). Through the end of the Cretaceous in the type locality of the Hell Creek Formation. Geological Society of America Special Paper, 503:173-208. DOI: 10.1130/2014.2503 (06)
https://doi.org/10.1130/2014.2503 (06)...
) confirm the difficulty in discriminating a preferable family to Cupressinocladus, considering their convergent characteristics shared with more than one conifer family. In extant conifers, besides the Cupressaceae, short and acute leaves that are oppositely arranged can also be found in the heterophilic shoots of Podocarpaceae (Page 1999Page C.N. 1999. Podocarpaceae. In: Judd W.S., Campbell C.S., Kellog E.A., Stevens P.F. (eds.). Plant Systematics: a phylogenetic approach. Massachusetts, Sinauer Associates, p. 332-346., Seward 2010Seward A.C. 2010. Fossil Plants: A Text-Book for students of botany and geology: Ginkgoales, Coniferales, Gnetales. New York, Cambridge University Press , v. 5, 545 p., Fontes & Dutra 2010Fontes D., & Dutra T.L. 2010. Paleogene imbricate-leaved podocarps from King George Island (Antarctica): assessing the geological context and botanical affinities. Revista Brasileira de Paleontologia, 13(3):189-204. DOI: 10.4072/rbp.2010.3.04
https://doi.org/10.4072/rbp.2010.3.04...
, Mao et al. 2012Mao K., Milne R.I., Zhang L., Peng Y., Liu J., Thomas P., Mill R.R., Renner S.S. 2012. Distribution of living Cupressaceae reflects the breakup of Pangea. Proceedings of the Natural Academy of Sciences USA, 109(20):7793-7798. DOI: 10.1073/pnas.1114319109
https://doi.org/10.1073/pnas.1114319109...
, Du et al. 2013Du B-X., Sun B-N., Ferguson D.K., Yan D-F., Dong C., Jin P-H. 2013. Two Brachyphyllum species from the Lower Cretaceous of Jiuquan Basin, Gansu Province, NW China and their affinities and palaeoenvironmental implications. Cretaceous Research, 41:242-255. DOI: 10.1016/j.cretres.2012.12.009
https://doi.org/10.1016/j.cretres.2012.1...
). In the absence of reproductive structures or preserved cuticles, we follow here the recommendation of Schweitzer (1974Schweitzer H.J. 1974. Die ‘’tertiaren” Koniferen Spitzbergens, Palaeontographica, 149B:1-89.) that proposes to include “cupressoid” foliages in Cupressinocladus genus and, for the herein commented reasons, with an uncertain familiar relation with the Cheirolepidiaceae.

?Araucariaceae/Cheirolepidiaceae cf. Brachyphyllum Lindley and Hutton emend. Harris 1979 ( Figs. 3E and 3F )

Material

UFRJ-DG1988-Pb, impression of a single, ultimate branch.

Description

Fragment of a planar branch, with short and broad (5 mm large) ramifications that are opposite to sub alternate, and disposed in 45º angles. The scale leaves show triangular contours and poorly visible radiated striae diverging from the leaf apex.

Remarks

The leaf shoot impression, with uniformly wide branches of opposite to subalternate arrangement, bearing weakly preserved leaves of obtuse apex appressed to the stem, and covered by longitudinal and radial divergent striations (Fig. 3E), indicates a resemblance with forms comprised in the Brachyphyllum morphogenus. In the genus, by the stout branch, approximates from the species B. obesum Heer (Yabe & Kubota 2004Yabe A., & Kubota K. 2004. Brachyphyllum obesum, newly discovered thermophilic conifer branch from the Lower Cretaceous Kitadani Formation of the Tetori Group, central Japan. Memoir of the Fukui Prefectural Dinosaur Museum, 3:23-29., Du et al. 2013Du B-X., Sun B-N., Ferguson D.K., Yan D-F., Dong C., Jin P-H. 2013. Two Brachyphyllum species from the Lower Cretaceous of Jiuquan Basin, Gansu Province, NW China and their affinities and palaeoenvironmental implications. Cretaceous Research, 41:242-255. DOI: 10.1016/j.cretres.2012.12.009
https://doi.org/10.1016/j.cretres.2012.1...
).

B. obesum is an important component of the paleotropical floras, including those from Northeastern Brazil, where is registered in all known lower Cretaceous deposits This is the case of the sedimentary successions from Japoatã and Riachuelo formations, in Sergipe-Alagoas Basin, Marizal Formation in the Tucano Basin, and Romualdo, Missao Velha, and Santana formations, from Araripe Basin (Teixeira 1948Teixeira C. 1948. Flora mesozoica Portuguesa. Pt I. Lisbon, Servicos Geológicos de Portugal, 118 p., Duarte 1985Duarte L. 1985. Vegetais fósseis da Chapada do Araripe, Brasil. Coletânia de Trabalhos Paleontológicos. Brasília, DNPM, 27, p. 557-563., Dutra et al. 2002Dutra T.L., Boardman D.R., Souza-Lima W. 2002. Os fósseis da bacia de Sergipe-Alagoas. Plantas: Gimnospermas. Phoenix, 46:1-4., Kunzmann et al. 2004Kunzmann L., Mohr B., Bernardes-de-Oliveira M.E.C. 2004. Gymnosperms from the Lower Cretaceous Crato Formation (Brazil). I. Araucariaceae and Lindleycladus (incertae sedis). Mitteilung aus dem Museum für Naturkunde Berlin, Geowissenschaftliche Reihe, 7:155-174. http://dx.doi.org/10.5194/fr-7-155-2004
http://dx.doi.org/10.5194/fr-7-155-2004...
, Sucerquia 2006Sucerquia P.A. 2006. Gimnospermas eocretáceas da Formação Crato, Bacia do Araripe, nordeste do Brasil. M.Sc Dissertation, Universidade de São Paulo, São Paulo, 108 p. DOI: 10.11606/D.44.2007.tde-22082007-105023
https://doi.org/10.11606/D.44.2007.tde-2...
, 2013Sucerquia P.A. 2013. Taxonomia, modos de preservação e fitogeografia de coníferas aptianas da região paleoequatorial da América do Sul. PhD Thesis, Instituto de Geociências da Universidade de São Paulo, São Paulo, 86 p., 13 pranchas., Lima et al. 2012Lima F.J., Saraiva A.A.F., Sayão J.M. 2012. Revisão da paleoflora das formações Missão Velha, Crato e Romualdo, Bacia do Araripe, nordeste do Brasil. Estudos Geológicos, 22(1):99-115. DOI: 10.18190/1980-8208/estudosgeologicos.v22n1p99-115
https://doi.org/10.18190/1980-8208/estud...
, Batista et al. 2017Batista M.E.P., Silva D.D.C., Sales M.A.F., Sá A.A., Saraiva A.A.F., Loiola M.I.B. 2017. New data on the stem and leaf anatomy of two conifers from the Lower Cretaceous of the Araripe Basin, northeastern Brazil, and their taxonomic and paleoecological implications. PLoS One, 12(3):e0173090. DOI: 10.1371/journal.pone.0173090
https://doi.org/10.1371/journal.pone.017...
).

In South America, diversified species of Brachyphyllum were also register to the rain shadow areas of the western Andean basins, Chile to Venezuela (Berry 1922Berry E.W. 1922. Contribution to the Paleobotany of Perú, Bolivia and Chile. The Johns Hopkins University Studies in Geology, 4:47-65. https://doi.org/10.5962/bhl.title.24727
https://doi.org/10.5962/bhl.title.24727...
, Archangelsky 1963Archangelsky S. 1963. A new Mesozoic flora from Ticó, Santa Cruz province, Argentina. British Museum (Natural History) Bulletin of Geology, 8:47-92., Baldoni 1979Baldoni A.M. 1979. Nuevos elementos paleoflorísticos de la tatoflora de la Fm. Spring Hill, límite Jurásico-Cretácico, subsuelo de Argentina, Australia y Sudáfrica. Ameghiniana, 16:103-119., Romero et al. 1995Romero L., Aldana M., Rangel C., Villavicencio E., Ramirez J. 1995. Boletin de fauna y flora fósil del Peru. Boletin 17, Serie D: Estudios Regionales, 332 p., Van Waveren et al. 2002Van Waveren I.M., van Konijnenburg-van Cittert J.H.A., van der Burgh J., Dilcher D.L. 2002. Macrofloral remains from the Lower Cretaceous of the Leiva region (Colombia). Scripta Geologica, 123:1-39., Monje-Dussán et al. 2016Monje-Dussán C., Martínez C., Escapa I., Madriñán S., 2016. Nuevos registros de helechos y coníferas cel Cretácico inferior en la cuenca del Valle superior del Magdalena, Colombia. Boletín de Geología, 38(4):29-42. DOI: 10.18273/revbol.v38n4-2016002
https://doi.org/10.18273/revbol.v38n4-20...
).

Still the familiar placement of the genus remains dubious, it has been normally included in the Cheirolepidiaceae, due to its morphological resemblance with the non-frenelopsid members of this family and the common presence of Classopollis-type pollen in the assemblages (Kerp 1990Kerp H. 1990. The study of fossil gymnosperms by means of cuticular analysis. Palaios, 5:548-569.). However, B. obesum from the Santana Formation was assigned to the Araucariaceae based on its cuticle micromorphology and wood features (Kunzmann et al. 2004Kunzmann L., Mohr B., Bernardes-de-Oliveira M.E.C. 2004. Gymnosperms from the Lower Cretaceous Crato Formation (Brazil). I. Araucariaceae and Lindleycladus (incertae sedis). Mitteilung aus dem Museum für Naturkunde Berlin, Geowissenschaftliche Reihe, 7:155-174. http://dx.doi.org/10.5194/fr-7-155-2004
http://dx.doi.org/10.5194/fr-7-155-2004...
, Sucerquia 2013Sucerquia P.A. 2013. Taxonomia, modos de preservação e fitogeografia de coníferas aptianas da região paleoequatorial da América do Sul. PhD Thesis, Instituto de Geociências da Universidade de São Paulo, São Paulo, 86 p., 13 pranchas., Batista et al. 2017Batista M.E.P., Silva D.D.C., Sales M.A.F., Sá A.A., Saraiva A.A.F., Loiola M.I.B. 2017. New data on the stem and leaf anatomy of two conifers from the Lower Cretaceous of the Araripe Basin, northeastern Brazil, and their taxonomic and paleoecological implications. PLoS One, 12(3):e0173090. DOI: 10.1371/journal.pone.0173090
https://doi.org/10.1371/journal.pone.017...
). The absence of those anatomical features in the preserved form of the Codó Formation, and the associated occurrence of both Classopollis and Araucariacites pollen grains in the Codó Formation (Lima 1982Lima M.R. 1982. Palinologia da Formação Codó na região de Codó. Boletim Instituto de Geociências da USP, 13:116-128.), make difficult to confirm its insertion into the Cheirolepidiaceae.

Spermatophyta incertae sedis CF1 morphotype( Figs. 4A-4F )

Material

UFRJ-DG 1457a-Pb, 1457b-Pb (holomorphotype sensuEllis et al. 2009Ellis B., Daly D., Hickey L.J., Johnson K.R., Mitchell J., Wilf P., Wing S.L. 2009. Manual of Leaf Architecture. Ithaca, Cornell University Press, 190 p.), referring to the part and counterpart (cast) of an isolated three lobed leaf; UFRJ 1983-Pb, 1994-Pb, partial impression of the leaf base, and UFRJ-DG 1986 Pb, has a preserved, folded leaf branch.

Description

Palmate dissected leaf (7 cm long and 5 cm wide), apparently coriaceous in texture, with three planarly disposed symmetrical lobes of linear-oblong outline and without basal constriction or a distinct petiole. The cuneate base is a continuum of the broad axis (0.6 cm wide, 2.5 cm long in the preserved portion) and does not have a visible sheath. The prominent central lobe (4.5 cm long, 1 cm wide) is separated from the lateral ones (diverging in angles of 35-40º) by deep sinusoidal incisions. Lobes with basal entire margins and irregular (serrate?) ones near apices. The ramified main vein (1 mm wide) splits when entering the lobes and ends at their apices without other visible ramifications. The very fine secondary veins (or striae) diverge at straight angles from the main veins, and do not reach the leaf margin. They probably end (they are not visible) in the weak marginal venation that merges at the apex. The black dots of iron oxi-hydroxides, organized in parallel rows over the blades, may represent aligned stomatal complexes (Fig. 4B).

Figure 4:
CF1 holomorphotype (UFRJ-DG 1457a-1457b Pb). (A, B) Mold and cast (mineralized) of a trilobed “birdfoot”-like leaf. The white arrow in B points to probable aligned stomata or glands over the central lobe. The black one indicates the fine marginal vein; (C) drawing of B, highlighting the weak visible secondary and marginal veins; (D, E) additional related leaf fragments, with partial axes and basal leaf impressions (UFRJ-DG 1983, 1994 Pb); (F) A folded leafy shoot showing an apparent additional unilobed leaf (UFRJ-DG 1986 Pb). Scale bars = 1 cm, except in figure F = 0.5 cm.

Remarks

CF1 is the most abundant morphotype in the Codó Formation flora, despite the partial preservation of the additional related materials. It shows a characteristic leaf type, of difficult affinity and comparison with the previously described fossils from Brazil, and even in its insertion in the high clades.

The close relative in morphological appeals are found in the shoots carrying decussate leaves with three symmetrical lobes (similar to a “birdfoot”) assigned to Novaolindia dubia identified in the Santana Formation beds (Kunzmann et al. 2007Kunzmann L., Mohr B.A.R., Bernardes-de-Oliveira M.E.C. 2007. Novaolindia dubia gen. et sp. nov., an enigmatic seed plant from the Early Cretaceous of northern Gondwana. Review of Palaeobotany and Palynology, 147:94-105. DOI: 10.1016/j.revpalbo.2007.06.004
https://doi.org/10.1016/j.revpalbo.2007....
, Plate I.7 and II 1-3). However, N. dubia, has simple and lobate leaves in the same axis, a feature that is impossible to be detected in the unique lamina herein preserved. Despite this limitation, a single basal leaf, visible in the folded leafy shoot related to CF1 (Fig. 4F), could correspond to those found in N. dubia. However, Kunzmann et al. (2007Kunzmann L., Mohr B.A.R., Bernardes-de-Oliveira M.E.C. 2007. Novaolindia dubia gen. et sp. nov., an enigmatic seed plant from the Early Cretaceous of northern Gondwana. Review of Palaeobotany and Palynology, 147:94-105. DOI: 10.1016/j.revpalbo.2007.06.004
https://doi.org/10.1016/j.revpalbo.2007....
) had no mention about the presence of veins or surface irregularities over the leaf blade of N. dubia. Based in the anatomical features (longitudinally aligned anomocytic to probably cyclocytic stomata) and the presence of capsule-like fertile organs, the authors propose a preferable relation of N. dubia with the gymnosperms. In the absence of organic materials preserved in CF1, and of venation features in N. dubia, more specific comparisons are difficult. Additionally, the CF1 leaves are nearly four times larger and broader lobes of nearly entire margins, distinct characters when compared with N. dubia.

Considering the presence of fine secondary veins, transversally disposed in relation to the primary veins, and of a continuous marginal vein (Fig. 4B), the Codó leaf seems to be more probably link to a dubious angiosperm. Among them, the North Hemisphere forms assigned to Araliaephyllum Fontaine (which is considered a Magnoliopsida) share features in common, like the trilobate palmate leaves with lanceolate lobes, and acute or rounded apices. For other side, the leaves in this Cretaceous morphogenus have distinct actinodromous venation and dentate margins in the middle-upper part of the blade (Greguš & Kvaček 2015Greguš J., Kvaček J. 2015. Revision of Cenomanian flora from the Maletín Sandstone. Acta Musei Nationalis Pragae, Series B, Historia Naturalis, 71(3-4):315-364. DOI 10.14446/AMNP.2015.315
https://doi.org/10.14446/AMNP.2015.315...
, Plates 14.3 and 15.4-6).

Another trilobed leaf from the Crato Member, Araripea floriferaMohr and Eklund (Mohr & Eklund 2003Mohr B., & Eklund H. 2003. Araripia florifera, a magnoliid angiosperm from the Lower Cretaceous Crato Formation (Brazil). Review of Palaeobotany and Palynology, 126:279-292. DOI: 10.1016/S0034-6667(03)00092-7
https://doi.org/10.1016/S0034-6667(03)00...
), was also considered to be in the angiosperms by the actinodromous venation. However, it has leaves with a strong decurrent base which is closer to the following CF3 morphotype herein described.

ANGIOSPERMS

? Nympheales CF2 morphotype cf. Pluricapellatia peltata B. Mohr, Bernardes-de-Oliveira & David W. Taylor 2008Mohr B., Bernardes-de-Oliveira M.E.C., Taylor D.W. 2008. Pluricarpellatia, a nymphaealean angiosperm from the Lower Cretaceous of northern Gondwana (Crato Formation, Brazil). Taxon, 57:1147-1158. ( Fig. 5A-B )

Material

A broad leaf impression associated with, but not connected to a bifurcate axis (UFRJ-DG1984-Pb), and an isolated ramified leaf branch (UFRJ-DG 1985-Pb).

Description

Impression (replica) of an eccentrically reniform-wide peltate leaf (3 cm long, 3.8 cm wide) diverging from a weakly jointed petiolate axis (Fig. 5A, white arrows) of 1.7 cm long and 0.2-0.3 mm wide, with an apparently very reduced sheath. The leaf base is truncated. The margins serrate to doubly serrate with short triangular and irregular teeth visible in a few sectors (Fig. 5A, black arrows). There is no evidence of organic connections between the superimposed leaf axis and the associated branch.

Figure 5:
(A, B) CF2 morphotype. A. reniform leaf (UFRJ-DG 1985-Pb) eccentrically inserted in a slender petiole and covered by dehydrated coats of iron minerals. Black arrows point to the weakly preserved triangular teeth more visible in the middle part of the margin. White arrows indicate the poorly developed (or preserved) nodes or grooves along the axes; (B) part of an associated axis with a short-ramified shoot (UFRJDG1984-Pb). Delicate striations over it could indicate a nodular character or the presence of aerenchymatous tissues; (C-E) CF3 morphotype (UFRJ-DG 1800-Pb), showing partially preserved pinnatilobed leaf, with decurrent lateral lobes of entire margins; (D) outline of C, highlighting the pinnate main vein and the irregular pattern of the secondary veins (semicraspedodromous?); (E) an additional cast of an incomplete fragment, showing the long and well-preserved swollen petiolate base (UFRJ-DG 1990-Pb). Scale bar = 1 cm.

Remarks

The morphological features of the CF2 leaf, with its apparently broad reniform blade and long axis, that seems connected to a cut in the base of the leaf, make this leaf morphotype similar to other eccentric peltate ones found in Lower Cretaceous beds, like, for example, Proteaephyllum reniforme Fontaine (Aptian) and Nelumbites Berry (Albian) of the Potomac Group (Doyle & Hickey 1976Doyle J.A., & Hickey L.J. 1976. Pollen and leaves from the Mid-Cretaceous Potomac group and their bearing on early angiosperm evolution. In: Beck C.B. (ed.). Origin and early evolution of angiosperms. New York, Columbia University Press, p. 139-206., Doyle & Upchurch Jr. 2014Doyle J.A., & Upchurch Jr. G.R. 2014. Angiosperm clades in the Potomac Group: what have we learned since 1977? Bulletin of the Peabody Museum of Natural History, 55(2):111-134. https://doi.org/10.3374/014.055.0203
https://doi.org/10.3374/014.055.0203...
). They are distributed along the tropical areas of southern Laurasia and northern Gondwana (Mohr & Rydin 2002Mohr B., & Rydin C. 2002. Trifurcatia flabellata n. gen. n. sp., a putative monocotyledon angiosperm from the Lower Cretaceous Crato Formation (Brazil). Mitteilungen Museum für Naturkunde Berlin Geowissenschaftliche Reihe, 5:335-344., Mohr et al. 2006Mohr B., Bernardes-de-Oliveira M.E.C., Georges B., Ouaja M. 2006. Palaeogeographic distribution and ecology of Klitzschophyllites, an early Cretaceous angiosperm in southern Laurasia and northern Gondwana. Cretaceous Research, 27:464-472. DOI: 10.1016/j.cretres.2005.08.001
https://doi.org/10.1016/j.cretres.2005.0...
, 2008Mohr B., Bernardes-de-Oliveira M.E.C., Taylor D.W. 2008. Pluricarpellatia, a nymphaealean angiosperm from the Lower Cretaceous of northern Gondwana (Crato Formation, Brazil). Taxon, 57:1147-1158., Doyle 2015Doyle J.A. 2015. Recognising angiosperm clades in the Early Cretaceous fossil record. Historical Biology, 27:414-429. DOI: 10.1080/08912963.2014.938235
https://doi.org/10.1080/08912963.2014.93...
).

With regard to the previously described specimens of Brazilian deposits (Araripe and Areado basins), they can partly be compared to Nymphaeites choffati Saporta, firstly described in Portugal (N. chofatiiTeixeira, 1948Teixeira C. 1948. Flora mesozoica Portuguesa. Pt I. Lisbon, Servicos Geológicos de Portugal, 118 p.), and latter in the Santana Formation (Duarte 1985Duarte L. 1985. Vegetais fósseis da Chapada do Araripe, Brasil. Coletânia de Trabalhos Paleontológicos. Brasília, DNPM, 27, p. 557-563.). To the Codó Formation it was until now the only macrofossil described, and considered relate with the Nymphaeaceae and the genus Nymphaeites Sternberg. emend. Heer by Duarte and Santos (1993Duarte L., & Santos R.S. 1993. Plant and fish megafossils from the Codó Formation, Parnaíba Basin, NE Brazil. Cretaceous Research, 14:735-746. https://doi.org/10.1006/cres.1993.1049
https://doi.org/10.1006/cres.1993.1049...
).

The distinctive characters between CF2 and the holotype of N. choffati, are the more fan-shaped leaf (2.5-4.5 cm in length and 2.5-3.0 cm wide) and the well preserved reticulate venation in the Santana Formation leaves. However, it can result of the distinct preservation modes and make difficult a more detailed comparison. The CF2 impression seems to represent a dorsoventrally deformed leaf or where the upper part of the margin was folded. No venation feature was preserved, probably because of its more coriaceous texture, which is highlighted by the cracked iron oxide-hydroxide deposits on top of the impression. They both share the same general leaf size and axis, dentate margins (but with broader teeth and glands in N. choffati) and a long petiolate axis with transversal lines (arrows in Fig. 5A). Duarte and Santos (1993Duarte L., & Santos R.S. 1993. Plant and fish megafossils from the Codó Formation, Parnaíba Basin, NE Brazil. Cretaceous Research, 14:735-746. https://doi.org/10.1006/cres.1993.1049
https://doi.org/10.1006/cres.1993.1049...
) have suggested that N. choffati had an aquatic habitat and link it to the Nympheales by the presence of root aggregates, with well-developed calyptras, and by the jointed petiolar axis, which have been interpreted as aerenchymatous tissues by the authors.

After Mohr and Rydin (2002Mohr B., & Rydin C. 2002. Trifurcatia flabellata n. gen. n. sp., a putative monocotyledon angiosperm from the Lower Cretaceous Crato Formation (Brazil). Mitteilungen Museum für Naturkunde Berlin Geowissenschaftliche Reihe, 5:335-344.) include N. chofatti in the synonym of Trifurcatia flabellata, preserved by reddish brown impressions in the Crato Member of the Santana Formation. They were based on their common leaves with serrate margins and conspicuous nodes and internodes in the axes. The authors pointed to their similar sizes, amplexicaule leaf blades, and the number of marginal triangular teeth they have (14-28 in N. chofatii and 20-25 in T. flabellata). However, in the diagnosis of T. flabellate, there was no mention or comparison made with N. choffati. Because of its major acrodromous/parallelodromous venation, its irregularly zigzagging secondary and transversal tertiaries, and because of the presence of gland like structures, T. flabellata is related to an ancient monocot that probably grows in a seasonally dry context.

In a revision of the early monocots distributed in the Cretaceous deposits of tropical areas, Mohr et al. (2006Mohr B., Bernardes-de-Oliveira M.E.C., Georges B., Ouaja M. 2006. Palaeogeographic distribution and ecology of Klitzschophyllites, an early Cretaceous angiosperm in southern Laurasia and northern Gondwana. Cretaceous Research, 27:464-472. DOI: 10.1016/j.cretres.2005.08.001
https://doi.org/10.1016/j.cretres.2005.0...
) included T. flabellata (and thus N. choffati from Portugal, Brazil and Northern Africa) in the diversity of KlitzschophyllitesLejal-Nicol (Lejal-Nicol 1987Lejal-Nicol A. 1987. Flores nouvelles du Paleozoique et du Mesozoique d’Egypte et du Soudan septentrional. Berliner Geowissenschaftliche Abhandlungen, A75:151-248.). A genus emendation was proposed in addition to its relationship with a putative monocot that adapted to drought and/or haline environments. For Mohr et al. (2006Mohr B., Bernardes-de-Oliveira M.E.C., Georges B., Ouaja M. 2006. Palaeogeographic distribution and ecology of Klitzschophyllites, an early Cretaceous angiosperm in southern Laurasia and northern Gondwana. Cretaceous Research, 27:464-472. DOI: 10.1016/j.cretres.2005.08.001
https://doi.org/10.1016/j.cretres.2005.0...
), the inclusion of N. choffati in the new genus was based on what previously Mohr and Rydin (2002Mohr B., & Rydin C. 2002. Trifurcatia flabellata n. gen. n. sp., a putative monocotyledon angiosperm from the Lower Cretaceous Crato Formation (Brazil). Mitteilungen Museum für Naturkunde Berlin Geowissenschaftliche Reihe, 5:335-344.) had been considering as an erroneous association of the Codó species with the Nymphaeaceae. The Brazilian specimens of T. flabellata from the Codó and Santana formations were associated with the K. flabellatus species, and were compared with the other two confirmed species, K. aegyptiacum Lejal-Nicol from Egypt (Barale & Ouaja 2002Barale G., & Ouaja M. 2002. La biodiversité végétale des gisements d’age Jurassique supérieure -Crétacé inférieur de Merbah El Asfer (Sud-Tunisien). Cretaceous Research, 23:707-737.) and K. choffatii, from Portugal and Tunisia. They were associated together due of their similar dentate margin and sizes (2-3 cm wide on average), except for the little Egypt form, which was slightly distinct in its leaf outline (Mohr et al. 2006Mohr B., Bernardes-de-Oliveira M.E.C., Georges B., Ouaja M. 2006. Palaeogeographic distribution and ecology of Klitzschophyllites, an early Cretaceous angiosperm in southern Laurasia and northern Gondwana. Cretaceous Research, 27:464-472. DOI: 10.1016/j.cretres.2005.08.001
https://doi.org/10.1016/j.cretres.2005.0...
, Fig. 2B and 2C). However, regarding the CF2 Codó morphotype herein described, and taking into account the eccentrically position of the reniform leaf in the axis the more probable and next affinity of CF2 is with the Klitzschophyllites choffatii specimens from Portugal (Mohr et al. 2006Mohr B., Bernardes-de-Oliveira M.E.C., Georges B., Ouaja M. 2006. Palaeogeographic distribution and ecology of Klitzschophyllites, an early Cretaceous angiosperm in southern Laurasia and northern Gondwana. Cretaceous Research, 27:464-472. DOI: 10.1016/j.cretres.2005.08.001
https://doi.org/10.1016/j.cretres.2005.0...
, Fig. 2B).

Gomez et al. (2009Gomez B., Coiffard C., Sender L.M., Martín-Closas C., Villanueva-Amadoz U., Ferrer J. 2009. Klitzschophyllites, aquatic basal Eudicots (Ranunculales?) from the Upper Albian (Lower Cretaceous) of Northeastern Spain. International Journal of Plant Sciences, 170:1075-1085. DOI: 10.1086/605117
https://doi.org/10.1086/605117...
), which later described specimens from northeast Spain, also consider that the Codó leaf must be related to this species. They also propose an emended diagnosis of K. choffatii (Saporta) and associate it with an aquatic basal Eudicot. Additionally, with regard to the Crato Member specimens, Gomez et al. (2009Gomez B., Coiffard C., Sender L.M., Martín-Closas C., Villanueva-Amadoz U., Ferrer J. 2009. Klitzschophyllites, aquatic basal Eudicots (Ranunculales?) from the Upper Albian (Lower Cretaceous) of Northeastern Spain. International Journal of Plant Sciences, 170:1075-1085. DOI: 10.1086/605117
https://doi.org/10.1086/605117...
) proposed to maintain its validity within the species Trifurcatia flabellata, because of its trifurcate axis and its relation with the monocts.

If the reniform character of CF2 leaf is confirmed by additional new materials it would also be comparable to the large eccentrically peltate leaves with crenulated margins that characterizes Pluricarpellatia peltataMohr, Bernardes de Oliveira and Taylor, and the “Nymphaeales Taxon A” of Mohr et al. (2008Mohr B., Bernardes-de-Oliveira M.E.C., Taylor D.W. 2008. Pluricarpellatia, a nymphaealean angiosperm from the Lower Cretaceous of northern Gondwana (Crato Formation, Brazil). Taxon, 57:1147-1158.), from the Crato Member, Araripe Basin. P. peltata is represented by a complete plant with aquatic shoots and flowers and in the variable leaf forms illustrated by Mohr et al. (2008Mohr B., Bernardes-de-Oliveira M.E.C., Taylor D.W. 2008. Pluricarpellatia, a nymphaealean angiosperm from the Lower Cretaceous of northern Gondwana (Crato Formation, Brazil). Taxon, 57:1147-1158.). With them, CF2 shares the size and irregular margins containing small teeth and differs only by the more slender and longitudinal striated petiole of P. peltata. Additionally, some specimens of P. peltata (Mohr et al. 2008Mohr B., Bernardes-de-Oliveira M.E.C., Taylor D.W. 2008. Pluricarpellatia, a nymphaealean angiosperm from the Lower Cretaceous of northern Gondwana (Crato Formation, Brazil). Taxon, 57:1147-1158., Fig. 3) exhibit bifurcated branches that resemble the isolated axis here preserved (Fig. 5B). Due to its carpel morphology and simple petiolate and peltate leaves of laminar placentation P. peltata was assigned to a Cabombaceae of herbaceous habit (Mohr et al. 2008Mohr B., Bernardes-de-Oliveira M.E.C., Taylor D.W. 2008. Pluricarpellatia, a nymphaealean angiosperm from the Lower Cretaceous of northern Gondwana (Crato Formation, Brazil). Taxon, 57:1147-1158.).

Finally, some common features also exist between CF2 and Jaguariba wiersemana (Coiffard, Mohr and Bernardes-de-Oliveira) and other Nympheales from the Santana Formation (Coiffard et al. 2013Coiffard C., Mohr B.A.R., Bernardes-de-Oliveira M.E.C. 2013. Jaguariba wiersemana gen. nov. et sp. nov., an Early Cretaceous member of crown group Nymphaeales (Nymphaeaceae) from northern Gondwana. Taxon, 62(1):141-151.), including the long petiole, which is eccentrically attached to a nano-to notophyllous elliptic-ovate lamina. They differ because the CF2 leaf is bigger and has irregular margins.

Magnollids CF3 morphotype cf. Araripia florifera Mohr and Eklund 2003Mohr B., & Eklund H. 2003. Araripia florifera, a magnoliid angiosperm from the Lower Cretaceous Crato Formation (Brazil). Review of Palaeobotany and Palynology, 126:279-292. DOI: 10.1016/S0034-6667(03)00092-7
https://doi.org/10.1016/S0034-6667(03)00...
( Figs. 5C-E )

Material

Basal-middle portion of a pinnate tri-lobed leaf (UFRJ-DG 1800-Pb); dispersed fragments from the basal part of the leaves (UFRJ-DG 1990-Pb; UFRJ-DG 1999-Pb).

Description

Pinnate tri-lobed notophyll leaf (6 cm wide, partly preserved), with symmetrical lobes separated by open and rounded sinus that have entire margins. The broad base forms a continuum with the also wide petiole (1 cm wide, 3 cm long) of the swollen base (Fig. 5E). The primary vein highlighted (10-5 mm wide) has two suprabasal and opposite inserted secondaries (5 mm large) that supply the lateral lobes and diverge from the primary vein in broad angles (60º), following a sharp convex course. An additional upper pair of secondaries is visible and diverges from the primary vein in a more acute angle (25º). Afterward, it curves upward in a semicraspedodromous pattern (Fig. 5D). The percurrent opposite tertiary veins have a sinuous course and cross the high order veins, which seem to end in the fine intramarginal vein.

Remarks

Pinnately lobed leaves (three or five lobes) that are similar to those of the CF3 morphotype have been reported in distinct Early Cretaceous deposits of Laurasia and Gondwana (Krassilov 1977Krassilov V.A. 1977. The origin of angiosperms. The Botanical Review, 43(1):143-176., Thomas & Spicer 1986Thomas B.A., & Spicer R.A. 1986. The Evolution and palaeobiology of land plants. London, Croom Helm, 309 p., Romero & Archangelsky 1986Romero E., & Archangelsky S. 1986. Early Cretaceous angiosperm leaves from Southern South America. Science, 234:1580-1582. DOI: 10.1126/science.234.4783.1580
https://doi.org/10.1126/science.234.4783...
, Crabtree 1987Crabtree D.R. 1987. Angiosperms of the northern Rocky Mountains: Albian to Campanian (Cretaceous) megafossil floras. Annals of the Missouri Botanical Garden, 74:707-747. https://doi.org/10.2307/2399448
https://doi.org/10.2307/2399448...
, Sun & Dilcher 2002Sun G., & Dilcher D.L. 2002. Early angiosperms from the Lower Cretaceous of Jixi, eastern Heilongjiang, China. Review of Palaeobotany and Palynology, 121:91-112. https://doi.org/10.1016/S0034-6667(02)00083-0
https://doi.org/10.1016/S0034-6667(02)00...
, Puebla 2009Puebla G.G. 2009. A new angiosperm leaf morphotype from the Early Cretaceous (Late Aptian) of San Luis Basin, Argentina. Ameghiniana, 46(3):557-566.). For Doyle (2015Doyle J.A. 2015. Recognising angiosperm clades in the Early Cretaceous fossil record. Historical Biology, 27:414-429. DOI: 10.1080/08912963.2014.938235
https://doi.org/10.1080/08912963.2014.93...
), in the Potomac Group, this kind of leaf architecture only appears in the basal middle Albian (Subzone IA), as part of the “platanoid” (Doyle & Hickey 1976Doyle J.A., & Hickey L.J. 1976. Pollen and leaves from the Mid-Cretaceous Potomac group and their bearing on early angiosperm evolution. In: Beck C.B. (ed.). Origin and early evolution of angiosperms. New York, Columbia University Press, p. 139-206., Doyle & Upchurch Jr. 2014Doyle J.A., & Upchurch Jr. G.R. 2014. Angiosperm clades in the Potomac Group: what have we learned since 1977? Bulletin of the Peabody Museum of Natural History, 55(2):111-134. https://doi.org/10.3374/014.055.0203
https://doi.org/10.3374/014.055.0203...
) or platanophyllic (Crabtree 1987Crabtree D.R. 1987. Angiosperms of the northern Rocky Mountains: Albian to Campanian (Cretaceous) megafossil floras. Annals of the Missouri Botanical Garden, 74:707-747. https://doi.org/10.2307/2399448
https://doi.org/10.2307/2399448...
) morphological complex, and coincides with the first appearance of the reticulate tricolpate pollen grains.

In Brazilian basins, such pinnate trilobed leaves are rare, but because of their suprabasal decurrent secondaries, they are comparable to some reproductive branches of Araripia floriferaMohr and Eklund, of the Crato flora (Mohr & Eklund 2003Mohr B., & Eklund H. 2003. Araripia florifera, a magnoliid angiosperm from the Lower Cretaceous Crato Formation (Brazil). Review of Palaeobotany and Palynology, 126:279-292. DOI: 10.1016/S0034-6667(03)00092-7
https://doi.org/10.1016/S0034-6667(03)00...
, Pls. 1 and 3.1), included in the Magnollid. However, A. florifera leaves might have an irregular number of lobes and craspedrodomous secondary veins. These features, unfortunately, are impossible to detect in this partially preserved margin of CF3. However, the upward curved upper pair of secondaries may suggest a semicraspedodromous venation. The main distinct characteristics between CF3 and A. florifera are the size of the lower leaves and their more irregular lobes (2-3 cm wide). However, these features usually vary in lobate leaves and can be controlled by environmental adaptations as well as ontogenetically. Mohr & Eklund (2003Mohr B., & Eklund H. 2003. Araripia florifera, a magnoliid angiosperm from the Lower Cretaceous Crato Formation (Brazil). Review of Palaeobotany and Palynology, 126:279-292. DOI: 10.1016/S0034-6667(03)00092-7
https://doi.org/10.1016/S0034-6667(03)00...
) compared A. florifera with Sassafras (Laurales) and with the leaf of Sassafras officinalis Nees Rugel.

The “leaf type 5” from Mohr and Friis (2000Mohr B., & Friis E.M. 2000. Early angiosperms from the Lower Cretaceous Crato Formation (Brazil), a preliminary report. International Journal of Plant Sciences, 161:S155-S167. https://doi.org/10.1086/317580
https://doi.org/10.1086/317580...
, Fig. 2G), another pinnately lobed leaf of the Santana Formation, shares some morphological features with CF3, like the full margins and the semicraspedodromous venation with the exmedial inflexion of the proximal pair of secondaries. However, it is different (or not preserved in CF3) in the high number of lobes (at least 7) of irregular size in the Crato Member leaves. Like in this case, this morphotype is represented by only one sample and has distinct types of round to ovate leaves, which are linked to the Nympheales, some of which are included later in the same species herein discussed with regard to the CF2 morphotype.

Additionally, it is important to call attention to the ternately platanoid lobed leaves initially mentioned, and its similarity to those present in Vitiphyllum. Vitiphyllum generally represents a basal eudicots (Doyle & Upchurch Jr. 2014Doyle J.A., & Upchurch Jr. G.R. 2014. Angiosperm clades in the Potomac Group: what have we learned since 1977? Bulletin of the Peabody Museum of Natural History, 55(2):111-134. https://doi.org/10.3374/014.055.0203
https://doi.org/10.3374/014.055.0203...
) which also share features with CF3. However, they normally characterize younger Albian levels of the mid-latitude Eastern Laurasia assemblages that have the first tricolpate pollen grains (Mohr & Eklund 2003Mohr B., & Eklund H. 2003. Araripia florifera, a magnoliid angiosperm from the Lower Cretaceous Crato Formation (Brazil). Review of Palaeobotany and Palynology, 126:279-292. DOI: 10.1016/S0034-6667(03)00092-7
https://doi.org/10.1016/S0034-6667(03)00...
, Doyle & Upchurch Jr. 2014Doyle J.A., & Upchurch Jr. G.R. 2014. Angiosperm clades in the Potomac Group: what have we learned since 1977? Bulletin of the Peabody Museum of Natural History, 55(2):111-134. https://doi.org/10.3374/014.055.0203
https://doi.org/10.3374/014.055.0203...
). This makes its presence in the Brazilian Equatorial basins less probable.

Concerning pinnate venation, suprabasal secondary and marginal veins, the CF3 leaf supports an affinity with the Magnollids, which was also proposed by Mohr and Eklund (2003Mohr B., & Eklund H. 2003. Araripia florifera, a magnoliid angiosperm from the Lower Cretaceous Crato Formation (Brazil). Review of Palaeobotany and Palynology, 126:279-292. DOI: 10.1016/S0034-6667(03)00092-7
https://doi.org/10.1016/S0034-6667(03)00...
) in relation to Araripea florifera. CF3 shows also a probable affinity with the Laurales and with “Sassafras” leaf type, considering the broad petiole and the inflexion in the basal secondaries (Little 1980Little E.L. 1980. The Audubon Society field guide to North American trees. New York, Albert A. Knopf, 778 p. ). Those morphological appeals, the swollen basal petiole and the membranaceous texture, seem to suggest a deciduous plant or a plant with a vine habit (Naidu 2012Naidu V.S.G.R. 2012. Hand Book on weed Identification. Jabalpur, India, Directorate of Weed Science Research, 354p., Pole 2015Pole M.S. 2015. The Distinct foliar physiognomy of the Late Cretaceous forests of New Zealand - probably deciduous. Gondwana Research, 27(3):1061-1067. DOI: 10.1016/j.gr.2014.02.009
https://doi.org/10.1016/j.gr.2014.02.009...
).

DISCUSSION

The tectonic and depositional context of the north Brazilian basins in the beginning of Cretaceous confirmed that they are part of a rift system derived from the breakup between South America and Africa. (Françolin & Szatmar 1987Françolin J.B.L., & Szatmar P. 1987. Mecanismo de rifteamento da porção oriental da margem norte brasileira. Revista Brasileira de Geociências, 17:196-207., Chang et al. 1992Chang H.K., Koswmann R.O., Figueiredo A.M.F., Bender A.A. 1992. Tectonics and stratigraphy of the East Brazil Rift system: an overview. Tectonophysics, 213:97-138. https://doi.org/10.1016/0040-1951(92)90253-3
https://doi.org/10.1016/0040-1951(92)902...
, Varejão et al. 2016Varejão F.G., Warren L.V., Perinotto J.A. de J., Neumann V.H., Freitas B.T., Almeida R.P., Assine M.L. 2016. Upper Aptian mixed carbonate-siliciclastic sequences from Tucano Basin, Northeastern Brazil: Implications for paleogeographic reconstructions following Gondwana break-up. Cretaceous Research, 67:44-58. DOI: 10.1016/j.cretres.2016.06.014
https://doi.org/10.1016/j.cretres.2016.0...
). This conditioning led to a sedimentary deposition that was controlled by the presence of marginal areas, and, during the upper Aptian, by seawater ingressions, probably through a still incipient Equatorial Atlantic gateway (Milani & Thomaz-Filho 2000Milani E.J., & Thomaz-Filho A. 2000. Sedimentary basins of South America. In: Cordani U.G., Milani E.J., Thomaz-Filho A., Campos D.A. (eds.). Tectonic evolution of South America. Rio de Janeiro, DNPM, p. 389-449., Rossetti et al. 2001Rossetti D.F., Góes A.M., Arai M. 2001. A passagem Aptiano-Albiano na Bacia do Grajaú. In: Rossetti D.F., Góes A.M., Truckenbrodt W. (eds.). O Cretáceo na Bacia de São Luís-Grajaú. Belém, Museu Paraense Emílio Goeldi, Coleção Friedrich Katzer, p. 101-117., Mizusaki et al. 2002Mizusaki A.M.P., Thomaz-Filho A., Milani E.J., Césero P. 2002. Mesozoic and Cenozoic igneous activity and its tectonic control in northeastern Brazil. Journal of South American Earth Sciences, 15:183-198. DOI: 10.1016/S0895-9811(02)00014-7
https://doi.org/10.1016/S0895-9811(02)00...
, Castro 2011Castro D.L. 2011. Gravity and magnetic joint modeling of the Potiguar Rift Basin (NE Brazil): basement control during Neocomian extension and deformation. Journal of South American Earth Sciences, 31:186-198. DOI: 10.1016/j.jsames.2011.01.005
https://doi.org/10.1016/j.jsames.2011.01...
).

The Early Cretaceous carbonate beds (e.g., the Marizal and Santana formations, respectively from the Recôncavo and Araripe basins, and the Codó Formation in the Parnaíba Basin), preserve fish related materials, gastropods and crustaceans, which are associated with plant fossils that can confirm the oceanic influence over and between the main lacustrine successions that conditioned the deposition (Mesner & Wooldrige 1964bMesner J.C., & Wooldridge L.C.P. 1964b. Maranhão paleozoic basin and Cretaceous coastal basins, north Brazil. AAPG Bulletin, 48(9):1475-1512., Darros de Matos 2000Darros de Matos, R.M. 2000. Tectonic evolution of the Equatorial South Atlantic. In: Mohriak W.U., Talwani M. (eds.). Atlantic Rifts and Continental Margins. Geophysical Monograph Series, AGU, p. 331-354.; Rossetti et al. 2001Rossetti D.F., Góes A.M., Arai M. 2001. A passagem Aptiano-Albiano na Bacia do Grajaú. In: Rossetti D.F., Góes A.M., Truckenbrodt W. (eds.). O Cretáceo na Bacia de São Luís-Grajaú. Belém, Museu Paraense Emílio Goeldi, Coleção Friedrich Katzer, p. 101-117., Amaral & Brito 2012Amaral C.R.L., & Brito P.M. 2012. A new Chanidae (Ostariophysii: Gonorynchiformes) from the Cretaceous of Brazil with affinities to Laurasian Gonorynchiforms from Spain. PLoS One, 7(5):e37247. DOI: 10.1371/journal.pone.0037247
https://doi.org/10.1371/journal.pone.003...
, Lindoso & Carvalho 2012Lindoso R.M., & Carvalho I. 2012. Crustáceos da Formação Codó (Bacia do Parnaíba, Brasil. In: Lopes F.C., Andrade A.I., Henriques M.H., Quinta-Ferreira M., Barata M.T., Pena dos Reis R. (eds.). Para entender a Terra: memórias e notícias de geociências no espaço lusófono. Portugal, Imprensa da Universidade de Coimbra, cap. 17, p. 171-177., Lindoso et al. 2016Lindoso R.M., Maisey J.G., Carvalho I.S. 2016. Ichthyofauna from the Codó Formation, Lower Cretaceous (Aptian, Parnaíba Basin), Northeastern Brazil and their paleobiogeographical and paleoecological significance. Palaeogeography, Palaeoclimatology, Palaeoecology, 447:53-64. DOI: 10.1016/j.palaeo.2016.01.045
https://doi.org/10.1016/j.palaeo.2016.01...
). More recently, the beds also give support to a Tethyan influence across the northern Brazilian areas (Arai 2014Arai M. 2014. Aptian/Albian (Early Cretaceous) paleogeography of the South Atlantic: a paleontological perspective. Brazilian Journal of Geology, 44(2):339-350. DOI: 10.5327/Z2317-4889201400020012
https://doi.org/10.5327/Z2317-4889201400...
). In the terrestrial and marginal areas, the palynological assemblages join pollen grains and spores that have a cosmopolitan distribution in South Laurasia, like Classopollis and Exesipollenites, associate to Sergipea and Tucanopolis, which are until now exclusive from the Gondwana (Tanrikulu et al. 2015Tanrikulu S., Doyle J., Delusina I. 2015. Pollen and spores of the Glen Rose Formation (Early Albian, Texas) and their implications for correlation of other sequences. GSA Annual Meeting in Baltimore, Maryland, (17-14).).

The Codó Formation macroflora herein described, and its associated microflora (Lima 1982Lima M.R. 1982. Palinologia da Formação Codó na região de Codó. Boletim Instituto de Geociências da USP, 13:116-128., 1989Lima M.R. 1989. Palinologia da Formação Santana (Cretáceo do Nordeste do Brasil). IV. Descrição sistemática dos polens das Turmas Plicates e Poroses, esporos, Incertae Sedis e microplancton marinho. Ameghiniana, 26:63-81., Pedrao et al. 1996Pedrão E., Barrilari I.M.R., Lima H.P. 1996. Palynological studies in the Cretaceous of the Parnaíba basin. In: Congresso Brasileiro de Geologia, 39. Annals… Salvador, Sociedade Brasileira de Geologia, p. 380-383.) confirm those data, despite their more limited preservation when compared with the well-preserved and known flora of the Santana Formation. Although its taxonomic placement was normally restricted to high rank clades, it had a vegetation sample that is not far from that which characterizes other Lower Cretaceous deposits, including Gnetales (cf. Drewria) and putative Cheirolepidiaceae/Araucariaceae?, which are associated with morphotypes that can attest to the conjunct occurrence of Nymphaeales, Magnoliids and other, still uncertain, early flowering plants.

Due to its general morphological features CF1 morphotype could be associated with both an angiosperms and a gymnosperms. The peltate round to ovate leaves of CF2 can be found in the Nympheaceae, in Monocots and in basal aquatic Eudicots. The morphotype “Spermatophyta incertae sedis”, for other side, have no comparison in the known fossil record and could represent a putative angiosperm. This information reinforces a previous unsuspected initial diversity of the lower Cretaceous angiosperms, and also its fast adaptation in the expanding lacustrine contexts and sunny open areas (in general with a dry climate), of the interior areas of tropical Pangea (Wing & Boucher 1998Wing S.L., & Boucher L.D. 1998. Ecological aspects of the Cretaceous flowering plant radiation. Annual Review of Earth and Planetary Sciences, 26:379-421. https://doi.org/10.1146/annurev.earth.26.1.379
https://doi.org/10.1146/annurev.earth.26...
, Gandolfo et al. 2000Gandolfo M.A., Nixon K.C., Crepet W. 2000. Monocotyledons: a review of their Cretaceous record. In: Wilson K.L., Morrison D.A. (eds.). Monocots: systematics and evolution. Australia, Csiro, p. 44-51., Martin-Closas et al. 2006Martin-Closas M., Delclos X., Gomez B., Soriano C. 2006. The biotic “lacustrine Mesozoic revolution”: new data from the Barremian of Iberia. In: Mesozoic Terrestrial Ecosystems International Symposium, 9, Manchester. Annals..., p. 168., Coiffard et al. 2007Coiffard C., Gomez B., Thevenard F. 2007. Early Cretaceous Angiosperm invasion of Western Europe and Major Environmental Changes. Annals of Botany, 100:545-553. DOI: 10.1093/aob/mcm160
https://doi.org/10.1093/aob/mcm160...
, Gee 2010Gee C. (ed.). 2010. Plants in Mesozoic Time: morphological innovations, phylogeny, ecosystems. Indiana: Indiana University Press, 374 p., Wang et al. 2016Wang W., Lin L., Xiang X-G., Ortiz R.C., Liu Y., Xiang K-L., Yu S-X., Xing Y-W., Chen Z-D. 2016. The rise of angiosperm-dominated herbaceous floras: insights from Ranunculaceae. Nature Scientific Reports, 6. DOI: 10.1038/srep27259
https://doi.org/10.1038/srep27259...
).

In the Codó Formation assemblage, palmate lobed leaves represent two (CF1 and CF3) of the three morphotypes that are probably related to the angiosperms and were also a common component of the Early Cretaceous assemblages. This has been known since the pioneering work of Berry (1919Berry E.W. 1919. Upper Cretaceous floras of the Easthern Gulf region in Tennessee, Mississipi, Alabama and Georgia. United States Geological Survey Professional Paper, 112.) and recognized by its role in age inferences (Doyle & Hickey 1976Doyle J.A., & Hickey L.J. 1976. Pollen and leaves from the Mid-Cretaceous Potomac group and their bearing on early angiosperm evolution. In: Beck C.B. (ed.). Origin and early evolution of angiosperms. New York, Columbia University Press, p. 139-206.) with regard to the phylogeny of the first angiosperms (Doyle & Endress 2010Doyle J.A., & Endress P.K. 2010. Integrating Early Cretaceous fossils into the phylogeny of living angiosperms: Magnoliidae and eudicots. Journal of Systematic Evolution, 48:1-35. DOI: 10.1111/j.1759-6831.2009.00058.x
https://doi.org/10.1111/j.1759-6831.2009...
, Doyle 2015Doyle J.A. 2015. Recognising angiosperm clades in the Early Cretaceous fossil record. Historical Biology, 27:414-429. DOI: 10.1080/08912963.2014.938235
https://doi.org/10.1080/08912963.2014.93...
). As observed by Crane and Upchurch Jr. (1987Crane P.R., & Upchurch Jr. G.R. 1987. Drewria potomacensis gen. et. sp. nov., an Early Cretaceous member of Gnetales from the Potomac Group of Virginia. American Journal of Botany, 74:1722-1736.), from work within levels of the Potomac Group Zone I of Virginia, conifers and angiosperms are still rare in Aptian assemblages and, as shown herein, are represented by a few fragmentary and incomplete samples. Many associated ferns suggest that some moister climates characterize the Southern United States at this moment. Based on this succession, which extends from the Aptian to the Cenomanian, Doyle (2015Doyle J.A. 2015. Recognising angiosperm clades in the Early Cretaceous fossil record. Historical Biology, 27:414-429. DOI: 10.1080/08912963.2014.938235
https://doi.org/10.1080/08912963.2014.93...
, Fig. 1) recently showed that palmate and trilobed morphotypes, will have been irradiated in the Albian and dispersed worldwide until the Cenomanian.

Trilobate leaves have occured since the archetypic aquatic plant Archaefructus from the Aptian of China (Sun et al. 2002Sun G., Ji Q., Dilcher D.L., Zheng S., Nixon K.C., Wang X. 2002. Archaefructaceae, a new basal angiosperm family. Science, 296:899-904. DOI: 10.1126/science.1069439
https://doi.org/10.1126/science.1069439...
) and led Doyle and Upchurch Jr. (2014Doyle J.A., & Upchurch Jr. G.R. 2014. Angiosperm clades in the Potomac Group: what have we learned since 1977? Bulletin of the Peabody Museum of Natural History, 55(2):111-134. https://doi.org/10.3374/014.055.0203
https://doi.org/10.3374/014.055.0203...
) to suggest that they predate (with exception of Vitiphyllum) the consistent presence of the tricolpate pollen of the Eudicots in the upper Aptian deposits of northern Gondwana, as well as in those from the Aptian-Albian boundary of Laurasia. Such a proposal is coherent with the likelihood-based analysis of Geeta et al. (2012Geeta R., Dávalos L.M., Levy A., Bohs L., Lavin M., Mummenhoff K., Sinha N., Wojciechowski M.F. 2012. Keeping it simple: flowering plants tend to retain, and revert to, simple leaves. New Phytologist, 193(2):481-493. DOI: 10.1111/j.1469-8137.2011.03951.x
https://doi.org/10.1111/j.1469-8137.2011...
), which confirms that the lobate character evolved early on in the leaves of the Eudicot stem lineage.

The peltate leaf with palinactinodromous venation of the CF3 morphotype (Fig. 5C-E), for example, differs from other related known fossils being analyzed. On the other hand, it shows ancestral features (like low-order veins, which are less organized or asymmetrically distributed along the leaf) that are also found worldwide. They were distributed in the Early Cretaceous Magnollids and in the first Eudicots (Feild et al. 2011Feild T.S., Brodribb T. J., Iglesis A., Chatelet D.S., Baresch A., Upchurch Jr. G.R., Gomez B., Mohr B., Coiffard B., Kvacek J., Jaramilo C. 2011. Fossil evidence for Cretaceous escalation in angiosperm leaf vein evolution. Proceedings of the National Academy of Sciences of the United States, 108(20):8363-8366. DOI: 10.1073/pnas.1014456108
https://doi.org/10.1073/pnas.1014456108...
, Sack & Scoffoni 2013Sack L., & Scoffoni C. 2013. Leaf venation: structure, function, development, evolution, ecology and applications in the past, present and future. New Phytologist, 198:983-1000. DOI: 10.1111/nph.12253
https://doi.org/10.1111/nph.12253...
, Zhang et al. 2015Zhang Z., Xia N., Gornall R.J. 2015. Leaf venation patterns in the genus Saxifraga (Saxifragaceae). Phytotaxa, 221(2):123-136. DOI: 10.11646/phytotaxa.221.2.2
https://doi.org/10.11646/phytotaxa.221.2...
). Other components of Codó and Potomac floras also exhibit low vein densities with values in the same range as in distinct non-angiosperm clades, supporting the idea that this were probably an ancestral feature of angiosperms, like proposed by Feild et al. (2011Feild T.S., Brodribb T. J., Iglesis A., Chatelet D.S., Baresch A., Upchurch Jr. G.R., Gomez B., Mohr B., Coiffard B., Kvacek J., Jaramilo C. 2011. Fossil evidence for Cretaceous escalation in angiosperm leaf vein evolution. Proceedings of the National Academy of Sciences of the United States, 108(20):8363-8366. DOI: 10.1073/pnas.1014456108
https://doi.org/10.1073/pnas.1014456108...
).

An analysis of the previous record shows that many lobate leaf designs were experienced by the flowering plants (Dutra & Batten 2000Dutra Y.L., & Batten D.J. 2000. Upper Cretaceous floras of King George Island, West Antarctica, and their palaeoenvironmental and phytogeographic implications. Cretaceous Research, 21:181-209. DOI: 10.1006/cres.2000.0221
https://doi.org/10.1006/cres.2000.0221...
, Pole 2015Pole M.S. 2015. The Distinct foliar physiognomy of the Late Cretaceous forests of New Zealand - probably deciduous. Gondwana Research, 27(3):1061-1067. DOI: 10.1016/j.gr.2014.02.009
https://doi.org/10.1016/j.gr.2014.02.009...
), and so difficulting its taxonomic insertion, especially when dealing with isolated leaves like here. Additionally, leaves can vary from entire to multiple lobate in the same branch or tree (Nicotra et al. 2011Nicotra A.B., Leigh A., Boyce C.K., Jones C.S., Niklas K.J., Royer D.L., Tsukaya H. 2011. The evolution and functional significance of leaf shape in the angiosperms. Functional Plant Biology, 38:535-552. https://doi.org/10.1071/FP11057
https://doi.org/10.1071/FP11057...
). This well-known leaf plasticity is today better understood. Considering the traditional forms for which they were conceived and the textures that were influenced by their habits and adaptations (or as a defence against herbivores), the important role of KNOX genes is now well recognized about its influence in this process (Royer et al. 2010Royer D.L., Miller I.M., Peppe D.J., Hickey L.J. 2010. Leaf economic traits from fossils support a weedy habit for early angiosperms. American Journal of Botany, 97(3):438-445. DOI: 10.3732/ajb.0900290
https://doi.org/10.3732/ajb.0900290...
, Nicotra et al. 2011Nicotra A.B., Leigh A., Boyce C.K., Jones C.S., Niklas K.J., Royer D.L., Tsukaya H. 2011. The evolution and functional significance of leaf shape in the angiosperms. Functional Plant Biology, 38:535-552. https://doi.org/10.1071/FP11057
https://doi.org/10.1071/FP11057...
, Dkhar & Pareek 2014Dkhar J., & Pareek A. 2014. What determines a leaf’s shape? EvoDevo, 5:47. DOI: 10.1186/2041-9139-5-47
https://doi.org/10.1186/2041-9139-5-47...
, Ferris et al. 2015Ferris K.G., Rushton T., Greenlee A.B., Toll K., Blackman B.K., Willis J.H. 2015. Leaf shape evolution has a similar genetic architecture in three edaphic specialists within the Mimulus guttatus species complex. Annals of Botany, 116:213-223. DOI: 10.1093/aob/mcv080
https://doi.org/10.1093/aob/mcv080...
).

On the other hand, the palmate-lobed leaves, which are common in extant herbs, vines and trees, grow today mostly along tropical and subtropical belts (Takayama et al. 2006Takayama K., Kajita T., Murata J., Tateishi Y. 2006. Phylogeography and genetic structure of Hibiscus tiliaceus - speciation of a pantropical plant with sea-drifted seeds. Molecular Ecology, 15:2871-2881. DOI: 10.1111/j.1365-294X.2006.02963.x
https://doi.org/10.1111/j.1365-294X.2006...
, Cheek 2007Cheek M.R. 2007. Malvaceae. In: Heywood V.H., Brummitt R.K., Culham A., Seberg O. (eds.). Flowering Plant Families of the World. Richmond, Royal Botanic Gardens Kew, p. 201-202., Maes et al. 2009Maes W.H., Trabucco A., Achten W.M.J., Muys B. 2009. Climatic growing conditions of Jatropha curcas L. Biomass and Bioenergy, 33:1481-1485. https://doi.org/10.1016/j.biombioe.2009.06.001
https://doi.org/10.1016/j.biombioe.2009....
), and could be a good proxy in detecting zones of the past that were submitted to this condition, in addition to the environmental adaptive processes in the fossil record. Regardless of its taxonomic classification, the small lobate leaves herein described suggest opportunistic deciduous, herbaceous or creeping habits, which colonize freshly disturbed substrates and have a climatic context subject to seasonal dry periods (Taylor & Hickey 1992Taylor D.W., & Hickey L.J. 1992. Phylogenetic evidence for the herbaceous origin of angiosperms. Plant Systematic and Evolution, 180:137-156., Royer et al. 2010Royer D.L., Miller I.M., Peppe D.J., Hickey L.J. 2010. Leaf economic traits from fossils support a weedy habit for early angiosperms. American Journal of Botany, 97(3):438-445. DOI: 10.3732/ajb.0900290
https://doi.org/10.3732/ajb.0900290...
, Nicotra et al. 2011Nicotra A.B., Leigh A., Boyce C.K., Jones C.S., Niklas K.J., Royer D.L., Tsukaya H. 2011. The evolution and functional significance of leaf shape in the angiosperms. Functional Plant Biology, 38:535-552. https://doi.org/10.1071/FP11057
https://doi.org/10.1071/FP11057...
, Jud 2015Jud N.A. 2015. Fossil evidence for a herbaceous diversification of early eudicot angiosperms during the Early Cretaceous. Proceedings of the Royal Society, 282. DOI: 10.1098/rspb.2015.1045
https://doi.org/10.1098/rspb.2015.1045...
).

Halamski (2013Halamski A.T. 2013. Latest Cretaceous leaf floras from southern Poland and western Ukraine. Acta Palaeontologica Polonica, 58(2):407-443. DOI: 10.4202/app.2011.0024
https://doi.org/10.4202/app.2011.0024...
), working with Cretaceous fossil plants, proposed that communities composed of palmate and lobed leaves (like Debeya), and those that are accompanied by the conifer Geinitzia reichenbachii (which shares some common characteristics with Cupressinocladus), support the idea of a xeromorphic flora that grows in disturbed environments along river systems. For Arens and Allen (2014Arens N.C., & Allen S.E. 2014. A florule from the base of the Hell Creek Formation in the type area of eastern Montana: implications for vegetation and climate. In: Wilson G.P., Clemens W.A., Horner J.R., Hartman J.H. (eds.). Through the end of the Cretaceous in the type locality of the Hell Creek Formation. Geological Society of America Special Paper, 503:173-208. DOI: 10.1130/2014.2503 (06)
https://doi.org/10.1130/2014.2503 (06)...
), Cupressinocladus is a genus characteristic of more drained areas around rivers or deltas, and Alvin (1983Alvin K.L. 1983. Reconstruction of a Lower Cretaceous conifer. Botanical Journal of the Linnean Society, 86:169-176. https://doi.org/10.1111/j.1095-8339.1983.tb00724.x
https://doi.org/10.1111/j.1095-8339.1983...
) considers that the Cheirolepidiaceae is an indicator of seasonally arid conditions.

Thus, as expressed by the types discussed in this study, and from other ones present in the Early Cretaceous floras of Brazil (Duarte & Santos 1993Duarte L., & Santos R.S. 1993. Plant and fish megafossils from the Codó Formation, Parnaíba Basin, NE Brazil. Cretaceous Research, 14:735-746. https://doi.org/10.1006/cres.1993.1049
https://doi.org/10.1006/cres.1993.1049...
, Ferreira et al. 2008Ferreira E.P., Carvalho M. de A., Lima H.P. 2008. Associação palinológica do Aptiano-Cenomaniano da bacia de São Luís (norte do Brasil). In: Simpósio de Paleobotânicos e Palinólogos, 12, Florianópolis. Boletim de Resumos, p. 70., Portela et al. 2014Portela H.A., Antonioli L., Dino R., Garcia M.J. 2014. Caracterização palinoflorística e paleoambiental da Formação santana (Cretáceo Inferior), poço 4-bo-1-pe, Bacia do Araripe, nordeste do Brasil. Revista Brasileira de Paleontologia, 17(3):363-372. DOI: 10.4072/rbp.2014.3.07
https://doi.org/10.4072/rbp.2014.3.07...
), the temporary resistant condition of the vegetation to drought and to hypersaline environments, proposed by Mohr et al. (2006Mohr B., Bernardes-de-Oliveira M.E.C., Georges B., Ouaja M. 2006. Palaeogeographic distribution and ecology of Klitzschophyllites, an early Cretaceous angiosperm in southern Laurasia and northern Gondwana. Cretaceous Research, 27:464-472. DOI: 10.1016/j.cretres.2005.08.001
https://doi.org/10.1016/j.cretres.2005.0...
), seems to be confirmed and coincides with the evaporitic depositional context of the Codó Formation.

In addition to the discussion regarding the plausibility of the first angiosperms having arrived in the tropical or in the high latitude areas, another impressive debate regards their initial adaptation to the environment. The herbaceous to shrubby habit here proposed in reference to CF1 and CF3, or/and an aquatic adaptation (in CF2), is suggested nowadays by many authors when dealing with the early angiosperms (based on the associated roots), and there has been a long-time debate about its adaptive evolution. An herbaceous to shrubby habit was inferred in relation to Drewria by Crane and Uchurch Jr. (1987Crane P.R., & Upchurch Jr. G.R. 1987. Drewria potomacensis gen. et. sp. nov., an Early Cretaceous member of Gnetales from the Potomac Group of Virginia. American Journal of Botany, 74:1722-1736.), in relation to Archaefructus by Sun et al. (2002Sun G., Ji Q., Dilcher D.L., Zheng S., Nixon K.C., Wang X. 2002. Archaefructaceae, a new basal angiosperm family. Science, 296:899-904. DOI: 10.1126/science.1069439
https://doi.org/10.1126/science.1069439...
), and in relation to the early Eudicots by Jud (2015Jud N.A. 2015. Fossil evidence for a herbaceous diversification of early eudicot angiosperms during the Early Cretaceous. Proceedings of the Royal Society, 282. DOI: 10.1098/rspb.2015.1045
https://doi.org/10.1098/rspb.2015.1045...
). As previously showed, the Aptian Codó flora shows its arrival from the near, wet coastal areas. It was submitted to a tropical and seasonally dry climate in a community composed mainly by Gnetales and conifers, as demonstrated in the macro and microflora, with the unique distinction of having ferns spores in the latter.

The contribution of Codó flora to age and correlations

Except by the lack of pteridophytes remains in the macroflora (despite present in the microflora, which also includes the upper Aptian Sergipea variverrucata of Regali & Santos, 1999Regali M.S.P., & Santos P.R.S. 1999. Palinoestratigrafia e geocronologia dos sedimentos Albo-Aptianos das bacias de Sergipe e de Alagoas. In: Simpósio sobre o Cretáceo do Brasil, 1. Abstract, p. 411-419.), an older age is supported to Codó Formation when compared with that of Santana Formation (Coimbra et al. 2002Coimbra J.C., Arai M., Carreño A.L. 2002. Biostratigraphy of Lower Cretaceous microfossils from the Araripe Basin, northeastern Brazil. Geobios, 35:687-698. https://doi.org/10.1016/S0016-6995(02)00082-7
https://doi.org/10.1016/S0016-6995(02)00...
; Heimhofer et al. 2008Heimhofer U., Hesselbo S.P., Pancost R.D., Martill D.M., Hochuli P.A., Guzzo J.V.P. 2008. Evidence for photic-zone euxinia in the Early Albian Santana Formation (Araripe Basin, NE Brazil). Terra Nova, 20:347-354. DOI: 10.1111/j.1365-3121.2008.00827.x
https://doi.org/10.1111/j.1365-3121.2008...
), like was propose by Lima (1982Lima M.R. 1982. Palinologia da Formação Codó na região de Codó. Boletim Instituto de Geociências da USP, 13:116-128.). This age inference shows to have a cosmopolitan character confirmed by the occurrence of similar assemblages, containing lobate leaves (3 to 5 lobes) with “bird-foot” design, in the basal Aptian Potomac floras. In Southernmost South America, palmate lobed leaves of putative angiosperms are also record (Archangelsky et al. 2009Archangelsky S., Barreda V., Passalia M.G., Gandolfo M., Prámparo M., Romero E., Cúneo R., Zamuner A., Iglesias A., Llorens M., Puebla G.G., Quattrocchio M., Volkheimer W. 2009. Early angiosperm diversification: evidence from southern South America. Cretaceous Research, 30:1072-1083. https://doi.org/10.1016/j.cretres.2009.03.001
https://doi.org/10.1016/j.cretres.2009.0...
) and at Albian arrive at the southern tip of Patagonia and northern Antarctic Peninsula (Rees & Smellie 1989Rees P.M., & Smellie J.L. 1989. Cretaceous angiosperms from an allegedly Triassic flora at Williams Point, Livingston Island, South Shetland Islands. Antarctic Science, 1(3):239-248. https://doi.org/10.1017/S0954102089000362
https://doi.org/10.1017/S095410208900036...
, Cantrill & Nichols 1996Cantrill D.J., & Nichols G.J. 1996. Taxonomy and palaeoecology of Early Cretaceous (Late Albian) angiosperm leaves from Alexander Island, Antarctica. Review of Palaeobotany and Palynology, 92:1-28. https://doi.org/10.1016/0034-6667(95)00105-0
https://doi.org/10.1016/0034-6667(95)001...
, Dutra & Batten 2000Dutra Y.L., & Batten D.J. 2000. Upper Cretaceous floras of King George Island, West Antarctica, and their palaeoenvironmental and phytogeographic implications. Cretaceous Research, 21:181-209. DOI: 10.1006/cres.2000.0221
https://doi.org/10.1006/cres.2000.0221...
, Cantrill 2001Cantrill D.J. 2001. Cretaceous high-latitude terrestrial ecosystems: an example from Alexander Island, Antarctica. Asociación Paleontológica Argentina, Publicación Especial, 7:39-44.).

The presence of the described macroflora in the Codó beds expands the knowledge about Early Cretaceous plant fossils in low-latitudes, which were well-known in Brazil only to the Araripe Basin. Also attest a critical moment of plant evolution (the evolutionary turnover from gymnosperm-to angiosperm-dominated ecosystems) and of profound paleogeographic changes. The breakup of the continuous landmasses, after this time interval, would have a direct influence on the vegetation taking into account their dependence of terrestrial areas for its dispersion.

CONCLUSION

The allochthonous-parautochthonous assemblage from the youngest levels of the Codó Formation, with forms related to the Gnetales, conifers and to those representing the stem group of angiosperms (Nympheales and Magnollids), give also support to the Aptian-Albian age proposed to its succession. Some other similar plants in the fossil record indicate a vegetation composed of aquatic and herbaceous/shrubby habits, growing in fluvial/deltaic, lacustrine, and coastal open areas, which were probably fed by river systems whose banks sheltered and allowed for the growing of conifers. Cyclical invasions of marine waters and climate variations between arid and wet conditions were inferred from palynomorphs and characterize the same upper levels that contain the macroflora. As noticed herein, analogous fossil assemblages characterize the paleotropical areas of Southern Laurasia and northern Gondwana at the same time interval.

The macro and microfloristic assemblage from the Codó Formation stands out partly from that of Araripe Basin, because of the initial presence of many pteridophytes (proven only in the microflora) and the almost complete lack of established Eudicots, which could have resulted from their slight age differences, or from their near coastal location, which was probably more influenced by oceanic humidity. The Early Cretaceous plant fossils of the Codó Formation, together with other Brazilian basins precede the first efforts of the break-up between North and South America, and Africa, and the arrival of the north Atlantic Ocean waters to Tethyan areas, ending with the terrestrial links between those lands. Therefore, with other floras of the Equatorial belt, they are aligned with the latter floras that show a cosmopolitan vegetation inherited of the Pangea times.

Although representing only a partial portrait of the original vegetation that grew in what today corresponds to the northeastern coast of Maranhão State, the herein discussed plant fossils and their associated facies, seem to support one of the numerous strategies suggested with regard to the first appearance of flowering plants and their subsequent diversification. Initially proposed by Doyle in 1969Doyle J.A. 1969. Cretaceous angiosperm pollen of the Atlantic coastal plain and its evolutionary significance. Journal of the Arnold Arboretum, 50(1):1-35. https://doi.org/10.5962/bhl.part.24686
https://doi.org/https://doi.org/10.5962/...
, they conceived of the emergence and initial radiation of angiosperms on disturbed, aquatic or dry areas, near the coastal plains. By a fortunate coincidence, the studied fossiliferous area of Maranhão State is today a good analogous to the paleoecological context that conditioned the grown of its plant fossils. Nowadays locates in a similar latitude to that occupied at the beginning of the Cretaceous, and still submitted to arid to semiarid conditions, their ephemeral floods and coastal lagoons, with scarce vegetation, are a good portrait of ancient times here aborded.

ACKNOWLEDGMENTS

We are deeply grateful to Dr. Ari Iglesias and the other anonymous reviewers, who made invaluable suggestions and comments along the review, which certainly have improved the text and its content. Financial support was provided by: the Foundation for Research and Scientific and Technological Development of Maranhão (Fundação de Amparo à Pesquisa e ao Desenvolvimento Científico e Tecnológico do Maranhão-FAPEMA), the Coordination for the Improvement of Higher Education Personnel (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-CAPES), the National Counsel for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico-CNPq), the Carlos Chagas Filho Foundation for Research Support in the State of Rio de Janeiro (Fundação Carlos Chagas Filho de Amparo à Pesquisa no Estado do Rio de Janeiro-FAPERJ) and the Center for Natural History and Archeology Research of Maranhão (Centro de Pesquisa de História Natural e Arqueologia do Maranhão-CPHNAMA).

REFERENCES

  • Alvin K.L. 1983. Reconstruction of a Lower Cretaceous conifer. Botanical Journal of the Linnean Society, 86:169-176. https://doi.org/10.1111/j.1095-8339.1983.tb00724.x
    » https://doi.org/10.1111/j.1095-8339.1983.tb00724.x
  • Amaral C.R.L., & Brito P.M. 2012. A new Chanidae (Ostariophysii: Gonorynchiformes) from the Cretaceous of Brazil with affinities to Laurasian Gonorynchiforms from Spain. PLoS One, 7(5):e37247. DOI: 10.1371/journal.pone.0037247
    » https://doi.org/10.1371/journal.pone.0037247
  • Antonioli L. 2001. Estudo palino-cronoestratigráfico da Formação Codó - Cretáceo Inferior do Nordeste Brasileiro. Thesis. Instituto de Geologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, 265 p.
  • Arai M. 2014. Aptian/Albian (Early Cretaceous) paleogeography of the South Atlantic: a paleontological perspective. Brazilian Journal of Geology, 44(2):339-350. DOI: 10.5327/Z2317-4889201400020012
    » https://doi.org/10.5327/Z2317-4889201400020012
  • Archangelsky S. 1963. A new Mesozoic flora from Ticó, Santa Cruz province, Argentina. British Museum (Natural History) Bulletin of Geology, 8:47-92.
  • Archangelsky S., Barreda V., Passalia M.G., Gandolfo M., Prámparo M., Romero E., Cúneo R., Zamuner A., Iglesias A., Llorens M., Puebla G.G., Quattrocchio M., Volkheimer W. 2009. Early angiosperm diversification: evidence from southern South America. Cretaceous Research, 30:1072-1083. https://doi.org/10.1016/j.cretres.2009.03.001
    » https://doi.org/10.1016/j.cretres.2009.03.001
  • Arens N.C., & Allen S.E. 2014. A florule from the base of the Hell Creek Formation in the type area of eastern Montana: implications for vegetation and climate. In: Wilson G.P., Clemens W.A., Horner J.R., Hartman J.H. (eds.). Through the end of the Cretaceous in the type locality of the Hell Creek Formation. Geological Society of America Special Paper, 503:173-208. DOI: 10.1130/2014.2503 (06)
    » https://doi.org/10.1130/2014.2503 (06)
  • Assine M.L. 1992. Análise estratigráfica da Bacia do Araripe, Nordeste do Brasil. Revista Brasileira de Geociências, 22:289-300.
  • Baldoni A.M. 1979. Nuevos elementos paleoflorísticos de la tatoflora de la Fm. Spring Hill, límite Jurásico-Cretácico, subsuelo de Argentina, Australia y Sudáfrica. Ameghiniana, 16:103-119.
  • Barale G., & Ouaja M. 2002. La biodiversité végétale des gisements d’age Jurassique supérieure -Crétacé inférieur de Merbah El Asfer (Sud-Tunisien). Cretaceous Research, 23:707-737.
  • Batista M.E.P., Silva D.D.C., Sales M.A.F., Sá A.A., Saraiva A.A.F., Loiola M.I.B. 2017. New data on the stem and leaf anatomy of two conifers from the Lower Cretaceous of the Araripe Basin, northeastern Brazil, and their taxonomic and paleoecological implications. PLoS One, 12(3):e0173090. DOI: 10.1371/journal.pone.0173090
    » https://doi.org/10.1371/journal.pone.0173090
  • Bernardes-de-Oliveira M.E.C., Mohr B., Dino R., Guerra-Sommer M. 2007. As floras mesofíticas brasileiras no cenário paleoflorístico mundial In: Carvalho I.S., Cassab R.C.T., Schwanke C., Carvalho M.A., Fernandes A.C.S., Rodrigues M.A.C., Carvalho M.S.S., Arai M., Oliveira M.E.Q. (eds.). Paleontologia: Cenários de Vida. Rio de Janeiro, Interciência, v. 1, p. 203-241.
  • Berry E.W. 1919. Upper Cretaceous floras of the Easthern Gulf region in Tennessee, Mississipi, Alabama and Georgia. United States Geological Survey Professional Paper, 112.
  • Berry E.W. 1922. Contribution to the Paleobotany of Perú, Bolivia and Chile. The Johns Hopkins University Studies in Geology, 4:47-65. https://doi.org/10.5962/bhl.title.24727
    » https://doi.org/10.5962/bhl.title.24727
  • Borges J. 1937. Estudos geológicos nos estados do Maranhão e Piauhy Relatorio Annual. Rio de Janeiro, Serviço Geológico e Mineralógico.
  • Brito P.M., Lindoso R.M., Carvalho I.S., Machado G.P. 2016. Discovery of Obaichthyidae gars (Holostei, Ginglymodi, Lepisosteiformes) in the Aptian Codó Formation of the Parnaíba Basin: remarks on paleobiogeographical and temporal range. Cretaceous Research, 59:10-17. https://doi.org/10.1016/j.cretres.2015.10.017
    » https://doi.org/10.1016/j.cretres.2015.10.017
  • Burger B.J., & Ward C.J. 2016. On the occurrence of fossil conifers with affinities to Geinitzia in the late Cretaceous (Campanian) Mesaverde Group, Williams Fork Formation of northeastern Utah, U.S.A. PeerJ Preprints, 4:e1862v1. DOI: 10.7287/peerj.preprints.1862v1
    » https://doi.org/10.7287/peerj.preprints.1862v1
  • Campbell D.F. 1949. Revised report on the reconnaissance geology of the Maranhão Basin Relatório Interno. Rio de Janeiro, Conselho Nacional do Petróleo, 117 p.
  • Cantrill D.J. 2001. Cretaceous high-latitude terrestrial ecosystems: an example from Alexander Island, Antarctica. Asociación Paleontológica Argentina, Publicación Especial, 7:39-44.
  • Cantrill D.J., & Nichols G.J. 1996. Taxonomy and palaeoecology of Early Cretaceous (Late Albian) angiosperm leaves from Alexander Island, Antarctica. Review of Palaeobotany and Palynology, 92:1-28. https://doi.org/10.1016/0034-6667(95)00105-0
    » https://doi.org/10.1016/0034-6667(95)00105-0
  • Castro D.L. 2011. Gravity and magnetic joint modeling of the Potiguar Rift Basin (NE Brazil): basement control during Neocomian extension and deformation. Journal of South American Earth Sciences, 31:186-198. DOI: 10.1016/j.jsames.2011.01.005
    » https://doi.org/10.1016/j.jsames.2011.01.005
  • Chang H.K., Koswmann R.O., Figueiredo A.M.F., Bender A.A. 1992. Tectonics and stratigraphy of the East Brazil Rift system: an overview. Tectonophysics, 213:97-138. https://doi.org/10.1016/0040-1951(92)90253-3
    » https://doi.org/10.1016/0040-1951(92)90253-3
  • Cheek M.R. 2007. Malvaceae. In: Heywood V.H., Brummitt R.K., Culham A., Seberg O. (eds.). Flowering Plant Families of the World Richmond, Royal Botanic Gardens Kew, p. 201-202.
  • Coiffard C., Gomez B., Thevenard F. 2007. Early Cretaceous Angiosperm invasion of Western Europe and Major Environmental Changes. Annals of Botany, 100:545-553. DOI: 10.1093/aob/mcm160
    » https://doi.org/10.1093/aob/mcm160
  • Coiffard C., Mohr B.A.R., Bernardes-de-Oliveira M.E.C. 2013. Jaguariba wiersemana gen. nov. et sp. nov., an Early Cretaceous member of crown group Nymphaeales (Nymphaeaceae) from northern Gondwana. Taxon, 62(1):141-151.
  • Coimbra J.C., Arai M., Carreño A.L. 2002. Biostratigraphy of Lower Cretaceous microfossils from the Araripe Basin, northeastern Brazil. Geobios, 35:687-698. https://doi.org/10.1016/S0016-6995(02)00082-7
    » https://doi.org/10.1016/S0016-6995(02)00082-7
  • Crabtree D.R. 1987. Angiosperms of the northern Rocky Mountains: Albian to Campanian (Cretaceous) megafossil floras. Annals of the Missouri Botanical Garden, 74:707-747. https://doi.org/10.2307/2399448
    » https://doi.org/10.2307/2399448
  • Crane P.R., & Upchurch Jr. G.R. 1987. Drewria potomacensis gen. et. sp. nov., an Early Cretaceous member of Gnetales from the Potomac Group of Virginia. American Journal of Botany, 74:1722-1736.
  • Darros de Matos, R.M. 2000. Tectonic evolution of the Equatorial South Atlantic. In: Mohriak W.U., Talwani M. (eds.). Atlantic Rifts and Continental Margins Geophysical Monograph Series, AGU, p. 331-354.
  • Dkhar J., & Pareek A. 2014. What determines a leaf’s shape? EvoDevo, 5:47. DOI: 10.1186/2041-9139-5-47
    » https://doi.org/10.1186/2041-9139-5-47
  • Doyle J.A. 1969. Cretaceous angiosperm pollen of the Atlantic coastal plain and its evolutionary significance. Journal of the Arnold Arboretum, 50(1):1-35. https://doi.org/10.5962/bhl.part.24686
    » https://doi.org/https://doi.org/10.5962/bhl.part.24686
  • Doyle J.A. 2015. Recognising angiosperm clades in the Early Cretaceous fossil record. Historical Biology, 27:414-429. DOI: 10.1080/08912963.2014.938235
    » https://doi.org/10.1080/08912963.2014.938235
  • Doyle J.A., & Endress P.K. 2010. Integrating Early Cretaceous fossils into the phylogeny of living angiosperms: Magnoliidae and eudicots. Journal of Systematic Evolution, 48:1-35. DOI: 10.1111/j.1759-6831.2009.00058.x
    » https://doi.org/10.1111/j.1759-6831.2009.00058.x
  • Doyle J.A., & Hickey L.J. 1976. Pollen and leaves from the Mid-Cretaceous Potomac group and their bearing on early angiosperm evolution. In: Beck C.B. (ed.). Origin and early evolution of angiosperms New York, Columbia University Press, p. 139-206.
  • Doyle J.A., & Upchurch Jr. G.R. 2014. Angiosperm clades in the Potomac Group: what have we learned since 1977? Bulletin of the Peabody Museum of Natural History, 55(2):111-134. https://doi.org/10.3374/014.055.0203
    » https://doi.org/10.3374/014.055.0203
  • Du B-X., Sun B-N., Ferguson D.K., Yan D-F., Dong C., Jin P-H. 2013. Two Brachyphyllum species from the Lower Cretaceous of Jiuquan Basin, Gansu Province, NW China and their affinities and palaeoenvironmental implications. Cretaceous Research, 41:242-255. DOI: 10.1016/j.cretres.2012.12.009
    » https://doi.org/10.1016/j.cretres.2012.12.009
  • Duarte L. 1959. Relatório da seção de paleontologia Relatório Anual do Diretor. Rio de Janeiro, DGM/DNPM, p. 167-194.
  • Duarte L. 1985. Vegetais fósseis da Chapada do Araripe, Brasil Coletânia de Trabalhos Paleontológicos. Brasília, DNPM, 27, p. 557-563.
  • Duarte L., & Santos R.S. 1993. Plant and fish megafossils from the Codó Formation, Parnaíba Basin, NE Brazil. Cretaceous Research, 14:735-746. https://doi.org/10.1006/cres.1993.1049
    » https://doi.org/10.1006/cres.1993.1049
  • Dutra T.L., Boardman D.R., Souza-Lima W. 2002. Os fósseis da bacia de Sergipe-Alagoas. Plantas: Gimnospermas. Phoenix, 46:1-4.
  • Dutra Y.L., & Batten D.J. 2000. Upper Cretaceous floras of King George Island, West Antarctica, and their palaeoenvironmental and phytogeographic implications. Cretaceous Research, 21:181-209. DOI: 10.1006/cres.2000.0221
    » https://doi.org/10.1006/cres.2000.0221
  • Ellis B., Daly D., Hickey L.J., Johnson K.R., Mitchell J., Wilf P., Wing S.L. 2009. Manual of Leaf Architecture Ithaca, Cornell University Press, 190 p.
  • Feild T.S., Brodribb T. J., Iglesis A., Chatelet D.S., Baresch A., Upchurch Jr. G.R., Gomez B., Mohr B., Coiffard B., Kvacek J., Jaramilo C. 2011. Fossil evidence for Cretaceous escalation in angiosperm leaf vein evolution. Proceedings of the National Academy of Sciences of the United States, 108(20):8363-8366. DOI: 10.1073/pnas.1014456108
    » https://doi.org/10.1073/pnas.1014456108
  • Ferreira E.P., Carvalho M. de A., Lima H.P. 2008. Associação palinológica do Aptiano-Cenomaniano da bacia de São Luís (norte do Brasil). In: Simpósio de Paleobotânicos e Palinólogos, 12, Florianópolis. Boletim de Resumos, p. 70.
  • Ferris K.G., Rushton T., Greenlee A.B., Toll K., Blackman B.K., Willis J.H. 2015. Leaf shape evolution has a similar genetic architecture in three edaphic specialists within the Mimulus guttatus species complex. Annals of Botany, 116:213-223. DOI: 10.1093/aob/mcv080
    » https://doi.org/10.1093/aob/mcv080
  • Fontes D., & Dutra T.L. 2010. Paleogene imbricate-leaved podocarps from King George Island (Antarctica): assessing the geological context and botanical affinities. Revista Brasileira de Paleontologia, 13(3):189-204. DOI: 10.4072/rbp.2010.3.04
    » https://doi.org/10.4072/rbp.2010.3.04
  • Françolin J.B.L., & Szatmar P. 1987. Mecanismo de rifteamento da porção oriental da margem norte brasileira. Revista Brasileira de Geociências, 17:196-207.
  • Gandolfo M.A., Nixon K.C., Crepet W. 2000. Monocotyledons: a review of their Cretaceous record. In: Wilson K.L., Morrison D.A. (eds.). Monocots: systematics and evolution Australia, Csiro, p. 44-51.
  • Gee C. (ed.). 2010. Plants in Mesozoic Time: morphological innovations, phylogeny, ecosystems. Indiana: Indiana University Press, 374 p.
  • Geeta R., Dávalos L.M., Levy A., Bohs L., Lavin M., Mummenhoff K., Sinha N., Wojciechowski M.F. 2012. Keeping it simple: flowering plants tend to retain, and revert to, simple leaves. New Phytologist, 193(2):481-493. DOI: 10.1111/j.1469-8137.2011.03951.x
    » https://doi.org/10.1111/j.1469-8137.2011.03951.x
  • Geinitz H.B. 1842. Charakteristik der Schichten und Petrefacten des sächsisch-böhmischen Kreidegebirges, 3 Heft: Die sächsisch-böhmische Schweiz, die Oberlausitz und das Innere von Böhmen, Index Petrefactarum. Dresden, Arnoldische Buchhandlung, 120 p.
  • Gomez B., Coiffard C., Sender L.M., Martín-Closas C., Villanueva-Amadoz U., Ferrer J. 2009. Klitzschophyllites, aquatic basal Eudicots (Ranunculales?) from the Upper Albian (Lower Cretaceous) of Northeastern Spain. International Journal of Plant Sciences, 170:1075-1085. DOI: 10.1086/605117
    » https://doi.org/10.1086/605117
  • Gomez B, Ewin T.A.M., Daviero-Gomez V. 2012. The conifer Glenrosa falcata sp. nov. from the Lower Cretaceous of Spain and its palaeoecology. Review of Palaeobotany and Palynology, 172:21-32. DOI: 10.1016/j.revpalbo.2012.01.009
    » https://doi.org/10.1016/j.revpalbo.2012.01.009
  • Gomez B., Martín-Closas C., Barale G., de Porta N.S., Thévenard F., Guignard F. 2002. Frenelopsis (Coniferales: Cheirolepidiacea) and related male organ genera from the Lower Cretaceous of Spain. Palaeontology, 45(5):997-1036. DOI: 10.1111/1475-4983.00273
    » https://doi.org/10.1111/1475-4983.00273
  • Greguš J., Kvaček J. 2015. Revision of Cenomanian flora from the Maletín Sandstone. Acta Musei Nationalis Pragae, Series B, Historia Naturalis, 71(3-4):315-364. DOI 10.14446/AMNP.2015.315
    » https://doi.org/10.14446/AMNP.2015.315
  • Halamski A.T. 2013. Latest Cretaceous leaf floras from southern Poland and western Ukraine. Acta Palaeontologica Polonica, 58(2):407-443. DOI: 10.4202/app.2011.0024
    » https://doi.org/10.4202/app.2011.0024
  • Heimhofer U., Hesselbo S.P., Pancost R.D., Martill D.M., Hochuli P.A., Guzzo J.V.P. 2008. Evidence for photic-zone euxinia in the Early Albian Santana Formation (Araripe Basin, NE Brazil). Terra Nova, 20:347-354. DOI: 10.1111/j.1365-3121.2008.00827.x
    » https://doi.org/10.1111/j.1365-3121.2008.00827.x
  • Hickey L.J. 1973. Classification of the architecture of dicotyledoneous leaves. American Journal of Botany, 60:17-33.
  • Hickey L.J., & Wolfe J.A. 1975. The bases of angiosperm phylogeny: vegetative morphology. Annals of the Missouri Botanical Garden, 62:538-589. https://doi.org/10.2307/2395267
    » https://doi.org/10.2307/2395267
  • Iglesias A., Zamuner A.B., Poiré D.G., Larriestra F. 2007. Diversity, taphonomy and palaeoecology of an angiosperm flora from the Cretaceous (Cenomanian-Coniacian) in Southern Patagonia, Argentina. Palaeontology, 50(2):445-466. DOI: 10.1111/j.1475-4983.2007.00639.x
    » https://doi.org/10.1111/j.1475-4983.2007.00639.x
  • Jud N.A. 2015. Fossil evidence for a herbaceous diversification of early eudicot angiosperms during the Early Cretaceous. Proceedings of the Royal Society, 282. DOI: 10.1098/rspb.2015.1045
    » https://doi.org/10.1098/rspb.2015.1045
  • Kerp H. 1990. The study of fossil gymnosperms by means of cuticular analysis. Palaios, 5:548-569.
  • Kimura T., Ohana T., Naito G. 1992. Cupressinocladus sp., newly found from the Lower Cretaceous Wakino Formation, West Japan. Bulletin of the Kitakyushu Museum of Natural History, 11:79-86.
  • Krassilov V.A. 1977. The origin of angiosperms. The Botanical Review, 43(1):143-176.
  • Kunzmann L. 2010. Geinitzia reichenbachii (Geinitz, 1842) Hollick and Jeffrey, 1909 and Sedites rabenhorstii Geinitz, 1842 (Pinopsida; Late Cretaceous) reconsidered and redescribed. Review of Palaeobotany and Palynology, 159:123-140. DOI: 10.1016/j.revpalbo.2009.11.006
    » https://doi.org/10.1016/j.revpalbo.2009.11.006
  • Kunzmann L., Mohr B., Bernardes-de-Oliveira M.E.C. 2004. Gymnosperms from the Lower Cretaceous Crato Formation (Brazil). I. Araucariaceae and Lindleycladus (incertae sedis). Mitteilung aus dem Museum für Naturkunde Berlin, Geowissenschaftliche Reihe, 7:155-174. http://dx.doi.org/10.5194/fr-7-155-2004
    » http://dx.doi.org/10.5194/fr-7-155-2004
  • Kunzmann L., Mohr B., Bernardes-de-Oliveira M.E.C., Wilde V. 2006. Gymnosperms from the Lower Cretaceous Crato Formation (Brazil). II. Cheirolepidiaceae. Fossil Record, 9:213-225. DOI: 10.1002/mmng.200600009
    » https://doi.org/10.1002/mmng.200600009
  • Kunzmann L., Mohr B.A.R., Bernardes-de-Oliveira M.E.C. 2007. Novaolindia dubia gen. et sp. nov., an enigmatic seed plant from the Early Cretaceous of northern Gondwana. Review of Palaeobotany and Palynology, 147:94-105. DOI: 10.1016/j.revpalbo.2007.06.004
    » https://doi.org/10.1016/j.revpalbo.2007.06.004
  • Kunzmann L., Mohr B.A.R., Bernardes-de-Oliveira M.E.C. 2009. Cearania heterophylla gen. nov. et sp. nov., a fossil gymnosperm with affinities to the Gnetales from the Early Cretaceous of northern Gondwana. Review of Palaeobotany and Palynology, 158:193-212. DOI: 10.1016/j.revpalbo.2009.09.001
    » https://doi.org/10.1016/j.revpalbo.2009.09.001
  • Kunzmann L., Mohr B.A.R., Wilde V., Bernardes-de-Oliveira M.E.C. 2011. A putative gnetalean gymnosperm Cariria orbiculiconiformis gen. nov. et spec. nov. from the Early Cretaceous of northern Gondwana. Review of Palaeobotany and Palynology, 165:75-95. DOI: 10.1016/j.revpalbo.2011.02.005
    » https://doi.org/10.1016/j.revpalbo.2011.02.005
  • Lejal-Nicol A. 1987. Flores nouvelles du Paleozoique et du Mesozoique d’Egypte et du Soudan septentrional. Berliner Geowissenschaftliche Abhandlungen, A75:151-248.
  • Lima E.A.A., & Leite J.F. 1978. Projeto de estudo global dos recursos minerais da bacia sedimentar do Parnaíba: integração geológico-metalogenética. Relatório Final, Etapa III. Recife, DNPM-CPRM, 16 v., 473 p.
  • Lima F.J., Saraiva A.A.F., Sayão J.M. 2012. Revisão da paleoflora das formações Missão Velha, Crato e Romualdo, Bacia do Araripe, nordeste do Brasil. Estudos Geológicos, 22(1):99-115. DOI: 10.18190/1980-8208/estudosgeologicos.v22n1p99-115
    » https://doi.org/10.18190/1980-8208/estudosgeologicos.v22n1p99-115
  • Lima M.R. 1982. Palinologia da Formação Codó na região de Codó. Boletim Instituto de Geociências da USP, 13:116-128.
  • Lima M.R. 1989. Palinologia da Formação Santana (Cretáceo do Nordeste do Brasil). IV. Descrição sistemática dos polens das Turmas Plicates e Poroses, esporos, Incertae Sedis e microplancton marinho. Ameghiniana, 26:63-81.
  • Lindoso R.M. 2016. A biota da Formação Codó (Aptiano da Bacia do Parnaíba), Nordeste do Brasil: aspectos paleoambientais e paleobiogeográficos. PhD Thesis, Instituto de Geologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Rio de Janeiro, 161 p.
  • Lindoso R.M., & Carvalho I. 2012. Crustáceos da Formação Codó (Bacia do Parnaíba, Brasil. In: Lopes F.C., Andrade A.I., Henriques M.H., Quinta-Ferreira M., Barata M.T., Pena dos Reis R. (eds.). Para entender a Terra: memórias e notícias de geociências no espaço lusófono. Portugal, Imprensa da Universidade de Coimbra, cap. 17, p. 171-177.
  • Lindoso R.M., Carvalho I.S., Medeiros M.A., Mendes I.D., Marques N.E., Brito R., Almeida C.M. 2013a. A megaflora da Formação Codó (Aptiano, Bacia do Parnaíba), nordeste do Brasil. In: 23º Congresso Brasileiro de Paleontologia, 23., Gramado. Annals.. Gramado, SBP, p. 175-176.
  • Lindoso R.M., Carvalho I.S., Medeiros M.A., Pereira A.A., Santos R.A.B., Mendes I.D., Brito J.M., Bôas I.V., Araújo M.N., Ferreira N.N. 2011. Novos sítios fossilíferos em carbonatos da Formação Codó (Aptiano-Albiano) da Bacia do Parnaíba, Maranhão, Brasil In: Carvalho I.S., Srivastava N.K., Strohschoen Jr. O.S., Lana C.C. (eds.). Paleontologia: Cenários de Vida. Rio de Janeiro, Interciência , p. 819-827.
  • Lindoso R.M., Carvalho I.S., Mendes I.D. 2013b. An isopod from the Codó Formation (Aptian of the Parnaíba Basin), Northeastern Brazil. Brazilian Journal of Geology, 43(1):16-21. DOI: 10.5327/Z2317-48892013000100003
    » https://doi.org/10.5327/Z2317-48892013000100003
  • Lindoso R.M., Maisey J.G., Carvalho I.S. 2016. Ichthyofauna from the Codó Formation, Lower Cretaceous (Aptian, Parnaíba Basin), Northeastern Brazil and their paleobiogeographical and paleoecological significance. Palaeogeography, Palaeoclimatology, Palaeoecology, 447:53-64. DOI: 10.1016/j.palaeo.2016.01.045
    » https://doi.org/10.1016/j.palaeo.2016.01.045
  • Lisboa M.A.R. 1914. The Permian geology of Northern Brazil. American Journal of Science, 37:425-443. DOI: 10.2475/ajs.s4-37.221.425
    » https://doi.org/10.2475/ajs.s4-37.221.425
  • Little E.L. 1980. The Audubon Society field guide to North American trees New York, Albert A. Knopf, 778 p.
  • Maes W.H., Trabucco A., Achten W.M.J., Muys B. 2009. Climatic growing conditions of Jatropha curcas L. Biomass and Bioenergy, 33:1481-1485. https://doi.org/10.1016/j.biombioe.2009.06.001
    » https://doi.org/10.1016/j.biombioe.2009.06.001
  • Maizatto J.R., Queiroz-Neto J.V., Ferreira E.P., Bahniuk A. 2011. Palinomorfos e ostracodes não-marinhos de afloramento da Formação Codó, Bacia do Parnaíba. In: Carvalho I.S., Srivastava N.K., Strohschoen Júnior O., Lana C.C. (eds.). Paleontologia: Cenários de Vida Rio de Janeiro, Interciência , v. 3, p. 367-e377.
  • Mao K., Milne R.I., Zhang L., Peng Y., Liu J., Thomas P., Mill R.R., Renner S.S. 2012. Distribution of living Cupressaceae reflects the breakup of Pangea. Proceedings of the Natural Academy of Sciences USA, 109(20):7793-7798. DOI: 10.1073/pnas.1114319109
    » https://doi.org/10.1073/pnas.1114319109
  • Martin-Closas M., Delclos X., Gomez B., Soriano C. 2006. The biotic “lacustrine Mesozoic revolution”: new data from the Barremian of Iberia. In: Mesozoic Terrestrial Ecosystems International Symposium, 9, Manchester. Annals.., p. 168.
  • McNeill J., Barrie F.R., Buck W.R., Demoulin V., Greuter W., Hawksworth D.L., Herendeen P.S., Knapp S., Marhold K., Prado W.F., Van Reine P.H., Smith G.F., Wiersema J.H. 2012. International Code of Nomenclature for algae, fungi, and plants (Melbourne Code): adopted by the Eighteenth International Botanical Congress Melbourne, Australia, July 2011. Regnum Vegetabile 154. Australia, Koeltz Scientific Books.
  • Mesner J.C., & Wooldridge L.C.P. 1964a. Estratigrafia das bacias paleozoicas e cretáceas do Maranhão. Boletim Técnico Petrobras, 7(2):137-164.
  • Mesner J.C., & Wooldridge L.C.P. 1964b. Maranhão paleozoic basin and Cretaceous coastal basins, north Brazil. AAPG Bulletin, 48(9):1475-1512.
  • Meyen S.V. 1987. Fundamentals of Paleobotany New York, Chapman & Hall, 431p.
  • Milanez F.R. 1935. Estudo de um dicotyledoneo fossil do Cretaceo. Rodriguésia, 1:82-89.
  • Milani E.J., & Thomaz-Filho A. 2000. Sedimentary basins of South America. In: Cordani U.G., Milani E.J., Thomaz-Filho A., Campos D.A. (eds.). Tectonic evolution of South America Rio de Janeiro, DNPM, p. 389-449.
  • Mizusaki A.M.P., Thomaz-Filho A., Milani E.J., Césero P. 2002. Mesozoic and Cenozoic igneous activity and its tectonic control in northeastern Brazil. Journal of South American Earth Sciences, 15:183-198. DOI: 10.1016/S0895-9811(02)00014-7
    » https://doi.org/10.1016/S0895-9811(02)00014-7
  • Mohr B., & Eklund H. 2003. Araripia florifera, a magnoliid angiosperm from the Lower Cretaceous Crato Formation (Brazil). Review of Palaeobotany and Palynology, 126:279-292. DOI: 10.1016/S0034-6667(03)00092-7
    » https://doi.org/10.1016/S0034-6667(03)00092-7
  • Mohr B., & Friis E.M. 2000. Early angiosperms from the Lower Cretaceous Crato Formation (Brazil), a preliminary report. International Journal of Plant Sciences, 161:S155-S167. https://doi.org/10.1086/317580
    » https://doi.org/10.1086/317580
  • Mohr B., & Rydin C. 2002. Trifurcatia flabellata n. gen. n. sp., a putative monocotyledon angiosperm from the Lower Cretaceous Crato Formation (Brazil). Mitteilungen Museum für Naturkunde Berlin Geowissenschaftliche Reihe, 5:335-344.
  • Mohr B., Bernardes-de-Oliveira M.E.C., Georges B., Ouaja M. 2006. Palaeogeographic distribution and ecology of Klitzschophyllites, an early Cretaceous angiosperm in southern Laurasia and northern Gondwana. Cretaceous Research, 27:464-472. DOI: 10.1016/j.cretres.2005.08.001
    » https://doi.org/10.1016/j.cretres.2005.08.001
  • Mohr B., Bernardes-de-Oliveira M.E.C., Loveridge R.F. 2007. The macrophyte flora of the Crato Formation In: Martill D.M., Bechly G., Loveridge R.F. (eds.). The Crato Fossil Beds of Brazil New York, Cambridge University Press, p. 537-565.
  • Mohr B., Bernardes-de-Oliveira M.E.C., Taylor D.W. 2008. Pluricarpellatia, a nymphaealean angiosperm from the Lower Cretaceous of northern Gondwana (Crato Formation, Brazil). Taxon, 57:1147-1158.
  • Monje-Dussán C., Martínez C., Escapa I., Madriñán S., 2016. Nuevos registros de helechos y coníferas cel Cretácico inferior en la cuenca del Valle superior del Magdalena, Colombia. Boletín de Geología, 38(4):29-42. DOI: 10.18273/revbol.v38n4-2016002
    » https://doi.org/10.18273/revbol.v38n4-2016002
  • Moraes Rego L.F. 1923. Reconhecimento geológico feito no estado do Maranhão Relatório Anual do Diretor. Serviço Geológico e Mineralógico, p. 74-77.
  • Moreau J.-D., Néraudeau D., Tafforeau P., Dépré É. 2015. Study of the histology of leafy axes and male cones of Glenrosa carentonensis sp. nov. (Cenomanian Flints of Charente-Maritime, France), using synchrotron microtomography linked with palaeoecology. PLoS One, 10(8):e0134515. DOI: 10.1371/journal.pone.0134515
    » https://doi.org/10.1371/journal.pone.0134515
  • Naidu V.S.G.R. 2012. Hand Book on weed Identification Jabalpur, India, Directorate of Weed Science Research, 354p.
  • Nicotra A.B., Leigh A., Boyce C.K., Jones C.S., Niklas K.J., Royer D.L., Tsukaya H. 2011. The evolution and functional significance of leaf shape in the angiosperms. Functional Plant Biology, 38:535-552. https://doi.org/10.1071/FP11057
    » https://doi.org/10.1071/FP11057
  • Page C.N. 1999. Podocarpaceae. In: Judd W.S., Campbell C.S., Kellog E.A., Stevens P.F. (eds.). Plant Systematics: a phylogenetic approach. Massachusetts, Sinauer Associates, p. 332-346.
  • Paz J.D., & Rossetti D.F. 2001. Reconstrução paleoambiental da Formação Codó (Aptiano), borda leste da Bacia do Grajaú, MA. In: Rossetti D.F., Góes A.M., Truckenbrodt W. (eds.). O Cretáceo Na Bacia de São Luís-Grajaú Belém, Museu Paraense Emílio Goeldi, Coleção Friedrich Katzer, p. 77-100.
  • Pedrão E., Barrilari I.M.R., Lima H.P. 1996. Palynological studies in the Cretaceous of the Parnaíba basin. In: Congresso Brasileiro de Geologia, 39. Annals… Salvador, Sociedade Brasileira de Geologia, p. 380-383.
  • Pole M.S. 1993. Early Miocene flora of the Manuherikia Group, New Zealand, 8. Nothofagus. Journal of the Royal Society of New Zealand, 23(4):329-344. https://doi.org/10.1080/03036758.1993.10721230
    » https://doi.org/10.1080/03036758.1993.10721230
  • Pole M.S. 2000. Mid-Cretaceous Conifers from the Eromanga Basin, Australia. Australian Systematic Botany, 13:153-197. https://doi.org/10.1071/SB99001
    » https://doi.org/10.1071/SB99001
  • Pole M.S. 2015. The Distinct foliar physiognomy of the Late Cretaceous forests of New Zealand - probably deciduous. Gondwana Research, 27(3):1061-1067. DOI: 10.1016/j.gr.2014.02.009
    » https://doi.org/10.1016/j.gr.2014.02.009
  • Pons D. 1988. Le Mésozoique de Colombie: macroflores et microflores. Paris, Cahier Micropaleontologie, CNRS, 168 p.
  • Portela H.A., Antonioli L., Dino R., Garcia M.J. 2014. Caracterização palinoflorística e paleoambiental da Formação santana (Cretáceo Inferior), poço 4-bo-1-pe, Bacia do Araripe, nordeste do Brasil. Revista Brasileira de Paleontologia, 17(3):363-372. DOI: 10.4072/rbp.2014.3.07
    » https://doi.org/10.4072/rbp.2014.3.07
  • Puebla G.G. 2009. A new angiosperm leaf morphotype from the Early Cretaceous (Late Aptian) of San Luis Basin, Argentina. Ameghiniana, 46(3):557-566.
  • Rees P.M., & Smellie J.L. 1989. Cretaceous angiosperms from an allegedly Triassic flora at Williams Point, Livingston Island, South Shetland Islands. Antarctic Science, 1(3):239-248. https://doi.org/10.1017/S0954102089000362
    » https://doi.org/10.1017/S0954102089000362
  • Regali M.S.P., & Santos P.R.S. 1999. Palinoestratigrafia e geocronologia dos sedimentos Albo-Aptianos das bacias de Sergipe e de Alagoas. In: Simpósio sobre o Cretáceo do Brasil, 1. Abstract, p. 411-419.
  • Regali M.S.P., Uesugui N., Santos A.S. 1974. Palinologia dos sedimentos meso-cenozóicos do Brasil (I). Boletim Técnico da Petrobras, 17(3):177-191.
  • Ricardi-Branco F., Torres M., Tavares S.S., Carvalho I.S., Tavares P.G.E., Campos A.C.A. 2013. Itajuba yansanae gen, and sp. nov. of Gnetales, Araripe Basin (Albian-Aptian) in Northeast Brazil. In: Zhang Y., Ray P. (eds.). Climate change and regional/local responses, chapter 7, p. 187-205. DOI: 10.5772/55704
    » https://doi.org/10.5772/55704
  • Romero E., & Archangelsky S. 1986. Early Cretaceous angiosperm leaves from Southern South America. Science, 234:1580-1582. DOI: 10.1126/science.234.4783.1580
    » https://doi.org/10.1126/science.234.4783.1580
  • Romero L., Aldana M., Rangel C., Villavicencio E., Ramirez J. 1995. Boletin de fauna y flora fósil del Peru. Boletin 17, Serie D: Estudios Regionales, 332 p.
  • Rossetti D.F., Góes A.M., Arai M. 2001. A passagem Aptiano-Albiano na Bacia do Grajaú. In: Rossetti D.F., Góes A.M., Truckenbrodt W. (eds.). O Cretáceo na Bacia de São Luís-Grajaú Belém, Museu Paraense Emílio Goeldi, Coleção Friedrich Katzer, p. 101-117.
  • Royer D.L., Miller I.M., Peppe D.J., Hickey L.J. 2010. Leaf economic traits from fossils support a weedy habit for early angiosperms. American Journal of Botany, 97(3):438-445. DOI: 10.3732/ajb.0900290
    » https://doi.org/10.3732/ajb.0900290
  • Sack L., & Scoffoni C. 2013. Leaf venation: structure, function, development, evolution, ecology and applications in the past, present and future. New Phytologist, 198:983-1000. DOI: 10.1111/nph.12253
    » https://doi.org/10.1111/nph.12253
  • Santos M.E.C.M., & Carvalho M.S.S. 2009. Paleontologia das bacias Parnaíba, Grajaú e São Luís Rio de Janeiro, CPRM, 215 p.
  • Schweitzer H.J. 1974. Die ‘’tertiaren” Koniferen Spitzbergens, Palaeontographica, 149B:1-89.
  • Sender L.M., Villanueva-Amadoz U., Diez J.B., Sanchez-Pellicer R., Bercovici A., Pons D., Ferrer J. 2012. A new uppermost Albian flora from Teruel province, northeastern Spain. Geodiversitas, 34(2):373-397. DOI: 10.5252/g2012n2a7
    » https://doi.org/10.5252/g2012n2a7
  • Seward A.C. 1919. Fossil Plants Cambridge, Cambridge University Press, v. 4, 543 p.
  • Seward A.C. 2010. Fossil Plants: A Text-Book for students of botany and geology: Ginkgoales, Coniferales, Gnetales. New York, Cambridge University Press , v. 5, 545 p.
  • Silva-Santos R. 1985. Paleoictiofauna da Formação Codó, Bacia do Parnaíba, NE do Brasil. In: Congresso Brasileiro de Paleontologia, 9, Fortaleza, Brasil. Resumos, p. 11.
  • Srinivasan V. 1992. Two new species of the conifer Glenrosa from the Lower Cretaceous of North America. Review of Palaeobotany and Palynology, 72:245-255. https://doi.org/10.1016/0034-6667(92)90029-G
    » https://doi.org/10.1016/0034-6667(92)90029-G
  • Srinivasan V. 1995. Conifers from the Puddledock locality (Potomac Group, Early Cretaceous) in eastern North America. Review of Palaeobotany and Palynology, 89:257-286. DOI: 10.1016/0034-6667(95)00010-8
    » https://doi.org/10.1016/0034-6667(95)00010-8
  • Stewart W.N., & Rothwell G.W. 1993. Paleobotany and the evolution of plants 2ª ed. United Kingdom, Cambridge University Press, 525 p.
  • Sucerquia P.A. 2006. Gimnospermas eocretáceas da Formação Crato, Bacia do Araripe, nordeste do Brasil M.Sc Dissertation, Universidade de São Paulo, São Paulo, 108 p. DOI: 10.11606/D.44.2007.tde-22082007-105023
    » https://doi.org/10.11606/D.44.2007.tde-22082007-105023
  • Sucerquia P.A. 2013. Taxonomia, modos de preservação e fitogeografia de coníferas aptianas da região paleoequatorial da América do Sul PhD Thesis, Instituto de Geociências da Universidade de São Paulo, São Paulo, 86 p., 13 pranchas.
  • Sun G., & Dilcher D.L. 2002. Early angiosperms from the Lower Cretaceous of Jixi, eastern Heilongjiang, China. Review of Palaeobotany and Palynology, 121:91-112. https://doi.org/10.1016/S0034-6667(02)00083-0
    » https://doi.org/10.1016/S0034-6667(02)00083-0
  • Sun G., Ji Q., Dilcher D.L., Zheng S., Nixon K.C., Wang X. 2002. Archaefructaceae, a new basal angiosperm family. Science, 296:899-904. DOI: 10.1126/science.1069439
    » https://doi.org/10.1126/science.1069439
  • Takayama K., Kajita T., Murata J., Tateishi Y. 2006. Phylogeography and genetic structure of Hibiscus tiliaceus - speciation of a pantropical plant with sea-drifted seeds. Molecular Ecology, 15:2871-2881. DOI: 10.1111/j.1365-294X.2006.02963.x
    » https://doi.org/10.1111/j.1365-294X.2006.02963.x
  • Tanrikulu S., Doyle J., Delusina I. 2015. Pollen and spores of the Glen Rose Formation (Early Albian, Texas) and their implications for correlation of other sequences. GSA Annual Meeting in Baltimore, Maryland, (17-14).
  • Taylor D.W., & Hickey L.J. 1992. Phylogenetic evidence for the herbaceous origin of angiosperms. Plant Systematic and Evolution, 180:137-156.
  • Taylor T.N., Taylor E.L., Krings M. 2009. Paleobotany: The Biology and Evolution of Fossil Plants. Burlington/London/San Diego/New York, Elsevier/Academic Press Inc., 1,230 p.
  • Teixeira C. 1948. Flora mesozoica Portuguesa Pt I. Lisbon, Servicos Geológicos de Portugal, 118 p.
  • Thomas B.A., & Spicer R.A. 1986. The Evolution and palaeobiology of land plants London, Croom Helm, 309 p.
  • Vakhrameev V.A. 1991. Jurassic and Cretaceous floras and climates of the Earth Cambridge: Cambridge University Press, 318 p.
  • Vallati P. 2013. Paleotropical pollen grains from the Neuquén Group, Patagonia, Argentina. Carnets de Géologie [Notebooks on Geology], L05:273-279.
  • Van Waveren I.M., van Konijnenburg-van Cittert J.H.A., van der Burgh J., Dilcher D.L. 2002. Macrofloral remains from the Lower Cretaceous of the Leiva region (Colombia). Scripta Geologica, 123:1-39.
  • Varejão F.G., Warren L.V., Perinotto J.A. de J., Neumann V.H., Freitas B.T., Almeida R.P., Assine M.L. 2016. Upper Aptian mixed carbonate-siliciclastic sequences from Tucano Basin, Northeastern Brazil: Implications for paleogeographic reconstructions following Gondwana break-up. Cretaceous Research, 67:44-58. DOI: 10.1016/j.cretres.2016.06.014
    » https://doi.org/10.1016/j.cretres.2016.06.014
  • Vaz P.T., Rezende N.G.A.M., Filho J.R.W., Travassos W.A.S. 2007. Bacia do Paraíba. Boletim de Geociências Petrobras, 15:253-263.
  • Wang W., Lin L., Xiang X-G., Ortiz R.C., Liu Y., Xiang K-L., Yu S-X., Xing Y-W., Chen Z-D. 2016. The rise of angiosperm-dominated herbaceous floras: insights from Ranunculaceae. Nature Scientific Reports, 6. DOI: 10.1038/srep27259
    » https://doi.org/10.1038/srep27259
  • Watson J., & Fisher H.L. 1984. A new conifer genus from the Lower Cretaceous Glen Rose Formation, Texas. Palaeontology, 27:719-727.
  • Weissert H., Lini A., Föllmi K.B., Kuhn O. 1998. Correlation of Early Cretaceous carbon isotope stratigraphy and platform drowning events: a possible link? Palaeogeography, Palaeoclimatology, Palaeoecology, 137:189-203. DOI: 10.1016/S0031-0182(97)00109-0
    » https://doi.org/10.1016/S0031-0182(97)00109-0
  • Willis K.J., & McElwain J.C. 2002. The evolution of plants Oxford, Oxford University Press, 287 p.
  • Wing S.L., & Boucher L.D. 1998. Ecological aspects of the Cretaceous flowering plant radiation. Annual Review of Earth and Planetary Sciences, 26:379-421. https://doi.org/10.1146/annurev.earth.26.1.379
    » https://doi.org/10.1146/annurev.earth.26.1.379
  • Yabe A., & Kubota K. 2004. Brachyphyllum obesum, newly discovered thermophilic conifer branch from the Lower Cretaceous Kitadani Formation of the Tetori Group, central Japan. Memoir of the Fukui Prefectural Dinosaur Museum, 3:23-29.
  • Yang Y., Lin L., Ferguson D.K. 2015. Parallel evolution of leaf morphology in gnetophytes. Organisms, Diversity & Evolution, 15:651-662. DOI: 10.1007/s13127-015-0226-6
    » https://doi.org/10.1007/s13127-015-0226-6
  • Zhang Z., Xia N., Gornall R.J. 2015. Leaf venation patterns in the genus Saxifraga (Saxifragaceae). Phytotaxa, 221(2):123-136. DOI: 10.11646/phytotaxa.221.2.2
    » https://doi.org/10.11646/phytotaxa.221.2.2
  • Zhou Z., Thévénard F., Barale G., Guignard G. 2000. A new xeromorphic conifer from the Cretaceous of East China. Palaeontology, 43(3):561-572. DOI: 10.1111/j.0031-0239.2000.00140.x
    » https://doi.org/10.1111/j.0031-0239.2000.00140.x
  • Zijlstra G., & Kvaček Z. 2010. (1924) Proposal to conserve the name Cupressinocladus against Libocedrites (fossil Coniferophyta). Taxon, 59(1):301. DOI: 10.2307/27757081
    » https://doi.org/10.2307/27757081

Publication Dates

  • Publication in this collection
    Jan-Mar 2018

History

  • Received
    20 May 2017
  • Accepted
    04 Jan 2018
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