Abstract
An anuran tadpole recovered from a late Miocene (Turolian, MN13) lacustrine diatomaceous Konservat-Lagerstätte deposit near Tresjuncos (Spain) was studied. X-ray diffraction, micro-Raman spectroscopy, scanning electron microscopy and energy dispersive X-ray spectroscopy analyses were completed with the aim of determining the sequence of diagenetic events that led to its preservation and fossilization. These analyses performed on the fossil, host rock and contact between them indicate that varied and successive diagenetic processes conditioned by microbial activity intervened in its fossilization. The tadpole was buried in the lake during a massive planktonic diatom sedimentation event. A layered microcrystalline calcite coating was found and likely originated from a microbial mat that acted as a protective general sarcophagus. A differentiated environment was generated in the carcass, explaining the presence of authigenic minerals that are absent in the surrounding diatomites. The fossil is mainly formed by spar calcite mosaics, showing unusual spherical pits interpreted as external moulds of coccoid bacteria; however, some may also be derived from dissolved melanosomes. Sulphate reduction, possibly coupled with the anaerobic oxidation of methane, may have promoted the formation of spar calcite within the organic network of the carcass. The occurrence of sulphate minerals in different zones of the fossil reveals that saline water was present during the anaerobic organic decomposition and the fossilization process. The genesis of fibrous Mg-rich clay minerals that cover the pitted calcite crystals could have been bioinduced or inorganic.
Resumen
Se estudia un renacuajo de anuro encontrado cerca de la localidad de Tresjuncos (España) en un depósito “Konservat-Lagerstätte” del Mioceno superior (Turoliense, MN13). Los análisis de difracción de rayos X, espectroscopia micro-Raman, microscopía electrónica de barrido y energía dispersiva, se realizaron para determinar la secuencia de eventos diagenéticos que condujeron a la preservación y fosilización. Los análisis han indicado que en la fosilización han intervenido diferentes procesos diagenéticos, condicionados por la actividad microbiana. Se deduce que el renacuajo fue enterrado durante un evento masivo de sedimentación lacustre de diatomeas planctónicas. Una envoltura de láminas de calcita microcristalina encontrada alrededor del fósil, se formaría por velos microbianos que actuaron como un sarcófago protector. En el cadáver se generó un ambiente diferente al de la roca caja, y que propició la génesis de minerales diagenéticos que no aparecen en las diatomitas. El fósil está formado por mosaicos de cristales de calcita espática con poros esféricos, interpretados como moldes externos de bacterias cocoides; sin embargo, no se descarta que algunos de ellos sean melanosomas disueltos. Procesos de sulfato-reducción y posiblemente también una oxidación anaeróbica del metano pudieron haber promovido la precipitación de calcita espática dentro de la materia orgánica del cadáver. La aparición de minerales sulfatados en diferentes zonas del fósil revela que aguas salinas estaban presentes durante la descomposición anaeróbica de la materia orgánica y el proceso de fosilización. La génesis de minerales fibrosos de arcilla, ricos en Mg, formados sobre los cristales de calcita, podría haber sido bioinducida o inorgánica.
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References
Allison, P. A. (1988). Konservat-Lagerstatten: cause and classification. Paleobiology,14, 331–344.
Allison, P. A., Maeda, H., Tuzino, T., & Maeda, Y. (2008). Exceptional preservation within Pleistocene lacustrine sediments of Shiobara, Japan. Palaios,23, 260–266.
Barden, H. E., Bergmann, U., Edwards, N. P., Egerton, V. M., Manning, P. L., Perry, S., et al. (2015). Bacteria or melanosomes? A geochemical analysis of micro-bodies on a tadpole from the Oligocene Enspel Formation of Germany. Palaeobiodiversity and Palaeoenvironments,95, 33–45.
Becker, U., Fernández-González, A., Prieto, M., Harrison, R., & Putnis, A. (2000). Direct calculation of thermodynamic properties of the barite/celestine solid solution from molecular principles. Physics and Chemistry of Minerals,27, 291–300.
Bennett, P. C., Hiebert, F. K., & Rogers, J. R. (2000). Microbial control of mineral-groundwater equilibria: macroscale to microscale. Hydrogeology Journal,8, 47–62.
Beyssac, O., Goffé, B., Petitet, J.-P., Froigneux, E., Moreau, M., & Rouzaud, J.-N. (2003). On the characterization of disordered and heterogeneous carbonaceous materials by Raman spectroscopy. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy,59, 2267–2276.
Bhatti, T. M., & Yawar, W. (2010). Bacterial solubilization of phosphorus from phosphate rock containing sulfur-mud. Hydrometallurgy,103, 54–59.
Boetius, A., Ravenschlag, K., Schubert, C. J., Rickert, D., Widdel, F., Gieseke, A., et al. (2000). A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature,407, 623.
Bonny, S. M., & Jones, B. (2007). Diatom-mediated barite precipitation in microbial mats calcifying at Stinking Springs, a warm sulphur spring system in northwestern Utah, USA. Sedimentary Geology,194, 223–244.
Briggs, D. E. G. (2003a). The role of biofilms in the fossilization of non-biomineralized tissues. In W. E. Krumbein, D. M. Paterson, & A. Zavarzin (Eds.), Fossil and recent biofilms (pp. 281–290). Dordrecht: Springer.
Briggs, D. E. G. (2003b). The role of decay and mineralization in the preservation of soft-bodied fossils. Annual Review of Earth and Planetary Sciences,31, 275–301.
Brumsack, H. J. (1986). The inorganic geochemistry of Cretaceous black shales (DSDP Leg 41) in comparison to modern upwelling sediments from the Gulf of California. In C.P. Summerhayes & N.J. Shackleton (Eds.), North Atlantic Palaeoceanography (pp. 47–462). Geological Society of America Special Publication.
Bustillo, M. Á. (2018). Formación de biodolomita durante un proceso de fosilización de insectos en diatomitas miocenas (Konservat-Lagerstätte Tresjuncos, Cuenca, España). Geogaceta,64, 127–130.
Bustillo, M. Á., Díaz-Molina, M., López-García, M. J., Delclòs, X., Peláez-Campomanes, P., Peñalver, E., et al. (2017). Geology and paleontology of Tresjuncos (Cuenca, Spain), a new diatomaceous deposit with Konservat-Lagerstätte characteristics from the European late Miocene. Journal of Iberian Geology,43, 395–411.
Calvo, J. P., Pozo, M., & Servant-Vildary, S. (1988). Lacustrine diatomite deposits in the Madrid Basin (Central Spain). Geogaceta,4, 14–17.
Dalla Vecchia, F. M., Venturini, S., & Tentor, M. (2002). The Cenomanian (late Cretaceous) Konservat-Lagerstatte of en Nammoûra (Kesrouâne province), northern Lebanon. Bollettino della Società Paleontologica Italiana,41, 51–68.
Darroch, S. A. F., Laflamme, M., Schiffbauer, J. D., & Briggs, D. E. G. (2012). Experimental formation of a microbial death mask. Palaios,27, 293–303.
Del Buey, P., Cabestreroa, O., Arroyo, X., & Sanz-Montero, M. E. (2018). Microbially induced palygorskite-sepiolite authigenesis in modern hypersaline lakes (Central Spain). Applied Clay Science. https://doi.org/10.1016/j.clay.2018.02.020.
Douglas, S. (2005). Mineralogical footprints of microbial life. American Journal of Science,305, 503–525.
García-Romero, E., & Suarez, M. (2010). On the chemical composition of sepiolite and palygorskite. Clay and Clay Minerals,58, 1–20.
Gardner, J. D. (2016). The fossil record of tadpoles. Fossil Imprint,72, 17–44.
Guerrero, C.M., López-Archilla, A.I. & Iniesto, M. (2016). Microbial mats and preservation. In: F.J. Poyato-Ariza & Á.D. Buscalioni (Eds.), Las Hoyas: a Cretaceous wetland. A multidisciplinary synthesis after 25 years of research on an exceptional fossil Lagerstätte from Spain (pp. 220–228). Munich: Dr. Friedrich Pfeil Verlag.
Hajós, M. (1986). Stratigraphy of Hungary’s Miocene diatomaceous earth deposits. Geologica Hungarica,49, 1–339.
Harding, I. C., & Chant, L. S. (2000). Self-sedimented diatom mats as agents of exceptional fossil preservation in the Oligocene Florissant lake beds, Colorado, United States. Geology,28, 195–198.
Holmer, M., & Storkholm, P. (2001). Sulphate reduction and sulphur cycling in lake sediments: a review. Freshwater Biology,46, 431–451.
Iniesto, M., Buscalioni, Á. D., Guerrero, M. C., Benzerara, K., Moreira, D., & López-Archilla, A. I. (2016). Involvement of microbial mats in early fossilization by decay delay and formation of impressions and replicas of vertebrates and invertebrates. Scientific Reports. https://doi.org/10.1038/srep25716.
Iniesto, M., Laguna, C., Florín, M., Guerrero, M. C., Chicote, A., Buscalioni, A. D., et al. (2015). The impact of microbial mats and their microenvironmental conditions in early decay of fish. Palaios,30, 792–801.
Iniesto, M., Villalba, I., Buscalioni, A. D., Guerrero, M. C., & López-Archilla, A. I. (2017). The effect of microbial mats in the decay of anurans with implications for understanding taphonomic processes in the fossil record. Scientific Reports,7, 1. https://doi.org/10.1038/srep45160.
Jennings, D. S., & Hasiotis, S. T. (2006). Taphonomic analysis of a dinosaur feeding site using geographic information systems (GIS), Morrison Formation, southern Bighorn Basin, Wyoming, USA. Palaios,21, 480–492.
Marnette, E. C., Hordijk, C., Breemen, N. V., & Cappenberg, T. E. (1992). Sulfate reduction and S-oxidation in a moorland pool sediment. Biogeochemistry,17, 123–143.
McNamara, M. E., Orr, P. J., Kearns, S. L., Alcala, L., Anadon, P., & Peñalver-Molla, E. (2010). Exceptionally preserved tadpoles from the Miocene of Libros, Spain: ecomorphological reconstruction and the impact of ontogeny upon taphonomy. Lethaia,43, 290–306.
McNamara, M., Orr, P. J., Kearns, S. L., Anadon, P., Alcala, L., & Peñalver-Molla, E. (2009). Soft tissue preservation in Miocene frogs from Libros (Spain): insights into the genesis of decay microenvironments. Palaios,24, 104–117.
McNamara, M. E., Van Dongen, B. E., Lockyer, N. P., Bull, I. D., & Orr, P. J. (2016). Fossilization of melanosomes via sulfurization. Palaeontology,59, 337–350.
Morales, J., Peláez-Campomanes, P., Abella, J., Montoya, P., Ruiz, F. J., Gibert, L., et al. (2013). The Ventian mammal age (latest Miocene): present state. Spanish Journal of Palaeontology,28, 149–160.
Nauhaus, K., Boetius, A., Krüger, M., & Iddel, F. (2002). In vitro demonstration of anaerobic oxidation of methane coupled to sulphate reduction in sediment from a marine gas hydrate area. Environmental Microbiology,4, 296–305.
Pesquero, M. D., Ascaso, C., Alcalá, L., & Fernández-Jalvo, J. (2010). A new taphonomic bioerosion in a Miocene lakeshore environment. Palaeogeography, Palaeoclimatology, Palaeoecology,295, 192–198.
Pilkington, J. B., & Simkiss, K. (1966). The mobilization of the calcium carbonate deposits in the endolymphatic sacs of metamorphosing frogs. Journal of Experimental Biology,45, 329–341.
Post, J. L., & Crawford, S. (2007). Varied forms of palygorskite and sepiolite from different geologic systems. Applied Clay Science,36, 232–244.
Purnell, M. A., Donoghue, P. J., Gabbott, S. E., McNamara, M. E., Murdock, D. J., & Sansom, R. S. (2018). Experimental analysis of soft-tissue fossilization: opening the black box. Palaeontology. https://doi.org/10.1111/pala.12360.
Roček, Z., Böttcher, R., & Wassersug, R. (2006). Gigantism in tadpoles of the Neogene frog Palaeobatrachus. Paleobiology,32, 666–675.
Singer, D. M., Griffith, E. M., Senko, J. M., Fitzgibbon, K., & Widanagamage, I. H. (2016). Celestine in a sulfidic spring barite deposit: a potential biomarker? Chemical Geology,440, 15–25.
Špinar, Z. V. (1976). Endolymphatic sacs and dorsal endocranial pattern: their significance for systematics and phylogeny of frogs. Věstník Ústředního Ústavu Geologického,51, 285–290.
Stockar, R., Adatte, T., Baumgartner, P. O., & Föllmi, K. B. (2013). Palaeoenvironmental significance of organic facies and stable isotope signatures: the Ladinian San Giorgio dolomite and Meride limestone of Monte San Giorgio (Switzerland, WHL UNESCO). Sedimentology,60, 239–269.
Toporski, J. K. W., Steele, A., Westall, F., Avci, R., Martill, D. M., & McKay, D. S. (2002). Morphologic and spectral investigation of exceptionally well-preserved bacterial biofilms from the Oligocene Enspel formation, Germany. Geochimica et Cosmochimica Acta,66, 1773–1791.
Van Dam, J. A., Aziz, H. A., Álvarez-Sierra, M., Hilgen, F. K., Van Den Hoek Ostende, L. W., Lourens, L. J., et al. (2006). Long period astronomical forcing of mammal turnover. Nature,443, 687–691.
Vinther, J. (2016). Fossil melanosomes or bacteria? A wealth of findings favours melanosomes: melanin fossilises relatively readily, bacteria rarely, hence the need for clarification in the debate over the identity of microbodies in fossil animal specimens. BioEssays,38, 220–225.
Walsh, J. J. (2013). On the nature of continental shelves. San Diego: Elsevier.
Wilby, P. R., & Briggs, D. E. G. (1997). Taxonomic trends in the resolution of detail preserved in fossil phosphatized soft tissues. Geobios,20, 493–502.
Acknowledgements
We are grateful to the technical staff of the Museo Nacional de Ciencias Naturales (MNCN, Madrid) laboratories, particularly R. González (XRD), L. Tormo, M. Furió, and A. Jorge (SEM, EDS, micro-Raman), and J. Muñoz (photography). We are grateful to A.D. Buscalioni, F. Ortega, J.L. Sanz, and J.L. Ortiz for recovering the fossil tadpole and for entrusting it to us. We thank R. Marquez for his help in translation and linguistic corrections. We also thank to Dr. Ana Alonso-Zarza and Dr. Miguel Iniesto for their detailed review of the manuscript. The present research was funded by the Spanish Project CGL2014-54818-P (Ministerio de Economía, Industria y Competitividad/FEDER, European Union).
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Bustillo, M.Á., Talavera, R.R. & Sanchiz, B. Biomineralization and diagenesis in a miocene tadpole: a mineralogical and taphonomic study. J Iber Geol 45, 609–624 (2019). https://doi.org/10.1007/s41513-019-00112-0
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DOI: https://doi.org/10.1007/s41513-019-00112-0