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Ecological Interactions in Cloudina from the Ediacaran of Brazil

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Ecological Interactions in Cloudina from the Ediacaran of Brazil www.nature.com/scientificreports OPEN Ecological interactions in Cloudina from the Ediacaran of Brazil: implications for the rise of animal Received: 19 September 2016 Accepted: 5 June 2017 biomineralization Published: xx xx xxxx Bruno Becker-Kerber1, Mírian Liza Alves Forancelli Pacheco2, Isaac Daniel Rudnitzki3, Douglas Galante4, Fabio Rodrigues5 & Juliana de Moraes Leme6 At the Ediacaran/Cambrian boundary, ecosystems witnessed an unparalleled biological innovation: the appearance of shelled animals. Here, we report new paleoecological and paleobiological data on Cloudina, which was one of the most abundant shelled animals at the end of the Ediacaran. We report the close association of Cloudina tubes with microbial mat textures as well as organic-rich material, syndepositional calcite and goethite cement between their flanges, thus reinforcing the awareness of metazoan/microorganism interactions at the end of the Ediacaran. The preservation of in situ tubes suggests a great plasticity of substrate utilization, with evidence of different life modes and avoidance behavior. Geochemical analysis revealed walls composed of two secondary laminae and organic sheets. Some walls presented boreholes that are here described as predation marks. Taken together, these data add further information regarding the structuring of shelled animal communities in marine ecosystems. The Ediacaran Period (635–541 Ma) was marked by the record of enigmatic macroscopic organisms. This time interval embraces the first record of fossilized animals, including biomineralizers (e.g., Namacalathus, Cloudina)1–3, and vagile bilateria (e.g., Kimberella)4, as well as their innovative ecological interactions, such as macrophagous predation and competition5, 6. These evolutionary novelties led to the escalation and systematic organization of food webs, guilds and niches7 during the Cambrian radiation8. It was the dawn of animal life. One of the key changes at the Ediacaran/Cambrian boundary was the disappearance of most macroscopic soft-bodied taxa. It is still a matter of discussion if this was a mass extinction event9. Nevertheless, recent data on Ediacaran soft-bodied organisms1 show that they were already declining in diversity, coinciding with the first appearance and spread of biomineralized metazoans (e.g., Cloudina, Namacalathus, Namapoikia) near the end of the Ediacaran – the ‘biotic replacement’ hypothesis. Biomineralization among animals was one of the most impactful innovations in the history of life, and it affected sedimentological regimes10 and biogeochemical cycles11 and led to the complexification of benthic eco- systems12–14 and ecological interactions5. Based on new data concerning modes of life, growth pattern/behavior, and the ecological interactions of the widespread genus Cloudina, we present new evidence that strengthens the role played by the new ecological opportunities (e.g., predation) that triggered unprecedented biotic changes (e.g., evolution of biomineralization among animals) near the Precambrian–Cambrian boundary. 1Programa de Pós-Graduação em Ecologia e Recursos Naturais, Universidade Federal de São Carlos, São Carlos (SP), Washington Luiz 325km, CEP 13565-905, Brazil. 2Departamento de Biologia, Universidade Federal de São Carlos - campus Sorocaba, Rod. João Leme dos Santos km 110, CEP 18052-780, Sorocaba (SP), Brazil. 3Departamento de Geologia, Universidade Federal de Ouro Preto, CEP 35400-000, Ouro Preto (MG), Brazil. 4Brazilian Synchrotron Light Laboratory, Brazilian Center for Research in Energy and Materials, Av. Giuseppe Maximo Scolfaro, 10000, CEP 13083-100, Campinas, Brazil. 5Departamento de Química, Instituto de Química, Universidade de São Paulo, Av. Prof. Lineu Prestes, 748, CEP 05508-000, São Paulo, Brazil. 6Instituto de Geociências, Universidade de São Paulo, São Paulo, Rua do Lago, 562, Cidade Universitária, CEP 05508-080, Brazil. Correspondence and requests for materials should be addressed to B.B.-K. (email: [email protected]) SCIENTIFIC REPORTS | 7: 5482 | DOI:10.1038/s41598-017-05753-8 1 www.nature.com/scientificreports/ Figure 1. Biolaminites associated with Cloudina. (A) Polished hand sample showing the layer with microbial mat textures (white double-headed arrow) and the dark mudstone (black double-headed arrow). (B) Polished hand sample with a microbial mat layer (white double-headed arrow) and a dark mudstone layer (black double-headed arrow) and Cloudina oriented vertically (top black arrow) or inside microbial mats (bottom black arrow). (C) Polished hand sample with oxidized microbial mat textures (white double-headed arrow) associated with a Cloudina tube in cross-section (black arrow) and a mudstone layer above (black double- headed arrow). (D) Polished hand sample with microbial mat textures (white double-headed arrow) showing dark crenulated laminations (black arrow). (E) Thin section of microbial mat textures (white double-headed arrows) with an oxidation front (white arrow) and interbedded mudstones (black double-headed arrow). (F) Thin section demonstrating the presence of Cloudina inside crenulated laminations (black square and white double-headed arrow) at the base and associated with Cloudina (top black arrows) in a mudstone layer (black double-headed arrow). (G) Magnification of the black square in (F), showing a small individual of Cloudina inside the laminations and showing internal tubular structures (white arrow). (H) Thin section of the microbial mat textures showing dark lamination (white arrow) overlying occasional quartz grains (black arrow). (I) Microfossil of cyanobacteria. (J) Dark crenulated laminations (white arrows) of the microbialite associated with Cloudina. (K) Raman mapping of the region shown in (J) showing the presence of the “G” band of kerogen (green) mainly in the laminations (white arrows). Scale bars (A,B) 1 cm, (C,E,F) 2 mm, (D, G,H) 1 mm, (I) 20 µm (J,K) 0.2 mm. Results Association with microbialites. Several (n = 291) autochthonous specimens of Cloudina were observed in association with microbialitic textures (biolaminites) in the dark limestones of the Tamengo Formation (Fig. 1; Supplementary Fig. S1). Petrographic analysis revealed crinkly lamination that trapped and bounded occasional SCIENTIFIC REPORTS | 7: 5482 | DOI:10.1038/s41598-017-05753-8 2 www.nature.com/scientificreports/ quartz grains (Fig. 1H). The remains of Cloudina tubes are occasionally found inside the microbial mat lam- inations (Fig. 1B,C,F,G). Internal tubular structures were observed in one specimen found inside the micro- bial textures (Fig. 1G). Raman mapping indicated major concentrations of kerogen in the darker laminations of the microbial mat texture (Fig. 1K). The biolaminites are well preserved, with distinct margins and laminations (Fig. 1). In one polished hand sample, it was possible to observe that the macrostructure is laterally continuous and consists of an alternation of light and dark submillimetric laminations with low and crenulated synoptical relief (Fig. 1A–D); it occasionally shows oxidized laminations (Fig. 1C,E). The mesostructure is characterized by a plane laminated profile, crenulated laminations and moderate laminar heritage. Modes of occurrence. In samples with microbial textures, Cloudina tubes do not present a preferred ori- entation with respect to possible current sorting and are not fragmented or disarticulated. In fact, they pres- ent well-preserved flanges (Fig. 2C,F; Supplementary Fig. 2D–F). They exhibit high sinuosity (Fig. 2C,D,L; Supplementary Fig. 2C,D) and drastic changes in growth direction (Fig. 2A–E; Supplementary Fig. 2A,C), which can be spatially related to other tubes (Fig. 2A–E). One specimen has two smaller tubes extending from the oral end of a bigger individual (Fig. 2J,K). Despite some vertically oriented tubes (Figs 1B, 2B,C,G–I), most of the specimens (82%, n = 88) are preserved in the horizontal to oblique position, either inside the microbial textures (Fig. 1B,G) or inside the mudstone that overlies the microbial mats (Fig. 2). Some horizontal to oblique tubes are sinuously transecting the bedding plane (Supplementary Fig. 2B). There are also specimens that change from an oblique/vertical orientation to a horizontal position (Fig. 2A,C) and vice versa (Fig. 2G,H). Only a few (n = 4) also presented closed and open flanges preferentially in opposite sides of the tube (bellow and above, respectively), but this is not a common feature (Fig. 2F). These fossils occur in an impure fine lime- stone, with microfacies defined as terrigenous mudstone. The matrix is represented by microspar and patches of sparry calcite that suggest a recrystallization of micrite. The terrigenous sediments consist of silt and fine sand grains, and they exclusively occur dispersed in the microspar matrix. The interior of the Cloudina tubes is filled mainly with sparry calcite and some microspar as cement obliteration. Microfossils were found in association with these autochthonous Cloudina (Fig. 1I). Calcite cement, goethite and organic-rich material inside the Cloudina flanges. Calcite cement and intercrystalline goethite are ubiquitous inside the flanges of most autochthonous Cloudina funnels (83% of the specimens; Fig. 3A–F,I), whereas siliciclastic grains are absent (Fig. 3C–E; Supplementary Fig. S2). The calcite cement occurs as patches of microspar-pseudospar (Fig. 3A,C,D; Supplementary Fig. S2) and patches of sparry calcite with equidimensional mosaic texture (Figs 2H and 3A,C–F). Goethite occurs as intercrystalline inside the sparry calcite
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