Oxidative conditions can lead to exceptional preservation through phosphatization

18 Exceptional preservation through phosphatization is primarily controlled by a reduction in 19 pH, favoring the precipitation of apatite over that of calcite. Laboratory experiments 20 suggested that phosphatization results from anoxic decay. Here we report results of the fine 21 scale mineralogical characterization of Cretaceous phosphatized fossils of teleost fishes and 22 crustaceans from the Jebel oum Tkout Lagerstätte (Morocco). Data collected using 23 complementary laboratory and synchrotron-based X-ray techniques reveal that oxidative 24 conditions were established at a certain step of decay. Supporting these conclusions are the 25 presence, covering and embedded in the phosphatized tissues, of Fe(III)-rich mineral 26 phases which precipitation was likely biologically-induced during decay. In contrast to the 27 general belief, the present study highlights that the establishment of oxidative conditions 28 during decay can be compatible with exceptional preservation of fossils through 29 phosphatization. 30


INTRODUCTION
Soft tissue phosphatization, i.e., calcium phosphate mineralization occurring prior to the degradational collapse of cellular tissues, provides the most spectacular fossils of animals, still exhibiting sub-cellular details (Martill, 1990;Briggs, 2003).Most of the time, soft tissues are pseudomorphically replaced by francolite (a carbonate-rich fluorapatite), as is the case of the ~110-Ma fossil fishes from the Santana Formation (Brazil) (Martill, 1988).Closed systems, such as those built by biofilms growing around carcasses, promote apatite precipitation by trapping phosphorus (Williams and Reimers, 1983;Martill, 1988;Briggs and Kear, 1993;Wilby et al., 1996).Laboratory experiments suggested that phosphatization results from a decay-induced fall in pH under anaerobic conditions, the decrease of pH being responsible for a switch from carbonate to phosphate precipitation (Allison, 1988;Briggs and Kear, 1993;Briggs and Wilby, 1996;Sagemann et al., 1999).However, authigenic phosphates such as francolite may precipitate under a number of redox conditions, including oxic to suboxic conditions (Föllmi, 1996 and references therein).Phosphatization requires a sufficient concentration of phosphorous (Martill, 1988;Briggs and Kear, 1993;Briggs, 2003), and oxic conditions are known to enhance the release of phosphorus (e.g., Meunier-Christmann et al., 1989).Here, we report an in-depth and in situ assessment of the redox conditions having prevailed during the phosphatization of "exceptionally preserved" Cretaceous fossils of fishes and crustaceans from the Jebel oum Tkout (OT1) Lagerstätte of Morocco.

METHODS
A combination of advanced characterization tools, including X-ray diffraction (XRD), scanning electron microscopy (SEM) and infrared (IR) spectroscopy was used to achieve a micro-geochemical characterization of a series of fossils.In addition, major-to-trace elemental composition was determined using synchrotron-based micro X-ray fluorescence (µXRF) mapping at a spatial resolution of 60-100 µm and at detection limits of a few tens of ppm (Gueriau et al., 2014(Gueriau et al., , 2018)).Samples were scanned in air using a 17.2 keV beam allowing detection of elements from chlorine to uranium.At this energy, X-rays penetrate up to a couple of millimeters, but only the XRF photons from the first hundreds of microns can be collected (see Gueriau et al., 2018).The deconvolution of µXRF data allowed estimating the concentrations of all detected elements, including rare earth elements (REEs) that were then normalized to the Post-Archean Australian Shale (PAAS) reference (McLennan, 1989) to reconstruct REE patterns, ratios and anomalies in the fossils at "local", submillimeter scales (Gueriau et al., 2015).Finally, the redox states of Fe and Ce were determined using synchrotronbased micro-X-ray absorption spectroscopy (µXAS) at a 3-10 µm spatial resolution.For Fe, continuous Cauchy wavelet transformation of the spectra was performed to establish a more robust determination of the speciation (Munoz et al., 2003).Additional details on Methods are provided in the GSA Data Repository 1 .

GEOLOGICAL AND PALEOENVIRONMENTAL CONTEXT
The Upper Cretaceous (Cenomanian, ~95 Myr) OT1 Lagerstätte from south-eastern Morocco (Fig. 1A) yielded a rich and well-preserved soft-bodied fauna including mollusks, insects, crustaceans, elasmobranchs and actinopterygian fishes embedded in a pale beige laminated mudstone carved by mudcracks (Fig. 1B), Absence of marine organisms and the presence of mudcracks, unionids and larvae of insects restricted to freshwater environments, strongly suggest a low-energy seasonally dried freshwater deposition environment (Dutheil, 1999;Garassino et al., 2006).A paleoenvironmental model of the whole Kem Kem area is available in Ibrahim et al. (2020).

MINERALOGY
Remarkably, many fossils exhibit soft tissues (muscles, cuticles and gills -Figs.1C-E -Dutheil, 1999;Garassino et al., 2006;Gueriau et al., 2015) pseudomorphically replaced by nanometric apatite crystallites (< 30 nm), identified as francolite by infrared spectroscopy (Fig. 1F).XRD analyses on oriented preparations indicate that illite and quartz are the main constituents of the bulk sedimentary matrix, with some interstratified illite-smectite minerals and kaolinite.These minerals are mainly detritic, except for the accordion-like automorphic crystals of kaolinite.Low trace metal concentrations (Fig. DR1C) with very low degree of enrichment (PAAS-normalized enrichment factors for V, Ni, Cu, Zn ⩽ 1.1, Cr ~1.9) and chemical index of alteration of ~78 (Nesbitt and Young, 1982; low range for illite), indicate very moderate weathering.The gypsum crystals filling mudcracks (Fig. 1B and DR5) and the Fe-rich clay minerals displaying plate-like or sheet-like habits forming roses on the sample surface (Figs.3I    and DR5) are clearly secondary (and rather recent), highlighting that sampling and storage conditions have slightly tampered with the samples.

REMAINS OF BIOFILMS
Just as in a textbook case, fossil biofilms can be observed at the OT1 Lagerstätte.They consist in large (tens of cm 2 ) reddish cracked films lying a few millimeters above each of the fossiliferous layers (Fig. 2A).The morphological similarities between these films (Figs.2B-D) and modern microbial mats (Fig. 2E) strengthened their identification as well-preserved fossil colonies of microorganisms.Moreover, the fossil skeleton, cuticles and soft tissues (white-toyellowish in color) are largely covered by similar reddish (to sometimes bluish) thin (a few tens of µm) films (Figs.1B, 1C, 3A and DR2A) that are interpreted as remains of biofilms.Reddish patches are also found embedded within the phosphatized soft tissues (Figs.3E, 3F and DR2C), suggesting that their precipitation was concomitant to phosphatization.

ANTIQUITY OF FE-OXIDES
The observed Fe(III) hydroxides surround skeleton tissues and are found around and within the phosphatized soft tissues (Figs.3E and DR2C), suggesting that they precipitated concomitantly with phosphatization.Although some Fe-rich phases in the matrix have been interpreted as resulting from the oxidation of pyrite (e.g., Gabbot et al., 2004;Osés et al., 2016), this is not the case for the observed Fe(III) hydroxides for which a primary origin is more likely.
Instead of a cubic or framboidal habit typical of pyrite weathering products, the observed Fe(III) hydroxides show a honeycomb-like morphology, rather typical of microbial mats (e.g., Frankel and Bazylinski, 2003;Davies et al., 2016).In particular, one can observe spherical imprints (Figs.3J, 3K and DR5), possibly created by coccoid-shaped bacteria (e.g., Iniesto et al., 2016) or gas bubbles having been produced within the microbial mats (e.g., Davies et al., 2016).The fossil biofilms discussed here have thus not been exposed to significant weathering or recrystallization.In other words, the observed Fe(III) hydroxides are likely primary, i.e. they precipitated during the life of the microbial mats, thereby indicating slightly oxic conditions during early diagenesis.

REDOX CONDITIONS DURING PHOSPHATIZATION
Synchrotron-based µXRF analyses of the phosphatic fossil tissues reveal that they incorporated REEs as well as strontium, yttrium and thorium (Fig. 3C).The incorporation of REEs, which substitute for calcium in apatite minerals, generally occurs during diagenesis, with concentrations increasing by three to four orders of magnitude within 10 3 -10 4 years depending on diagenetic conditions (Herwartz et al., 2013).The obtained REE patterns display a very limited enrichment in intermediate REEs ("bell-shaped" patterns) and a slightly negative Ce anomaly (Fig. DR4A; Gueriau et al., 2015).The PAAS-normalized La/Yb vs La/Sm values confirm that the fossils investigated underwent very limited weathering and recrystallization (Fig. 3D; Reynard et al., 1999;Lécuyer et al., 2003).The observed negative Ce anomaly thus reflects the early diagenetic redox conditions of burial (German and Elderfield, 1990) and points to slightly oxic conditions, consistent with the precipitation of Fe(III) hydroxides.Ce L3-edge spectroscopy confirms that Ce has a mixed valence (Gueriau et al., 2015), with oxidized Ce (i.e., Ce(IV)) contributing to 20 at.% of the total Ce (Fig. DR4B).

CONCLUSION
Instead of a fall in pH under anoxic conditions, the fine-scale micro-geochemical characterization conducted here strongly suggests that (slightly) oxic conditions prevailed during phosphatization.This conclusion is fully consistent with recent experiment results evidencing that chemical microenvironments generated by microbial mats may turn oxic after several weeks despite initially anoxic conditions (Iniesto et al., 2015).One could argue that the observed Fe(III) hydroxides may have been produced by anaerobic neutrophilic iron oxidizers (e.g., Miot et al., 2009;Hedrich et al., 2011).This would not be inconsistent with the present interpretation, i.e. the establishment of slightly oxic conditions during phosphatization, since neutrophilic iron oxidizers require the presence of nitrates to survive, i.e., slightly oxic conditions (anaerobic and anoxic are not strict synonyms).Altogether, in contrast to the standard view, the present results establish that exceptional preservation through phosphatization and oxidative conditions are not antithetic.Note the presence of another, slightly younger and marine Lagerstätte at Gara Sbaa (Martill et al., 2011), ca. 15 km southwest of OT1.B: Optical photograph of a gray illitic layer exhibiting mudcracks and topped by a reddish microbial mat.In the center, a paraclupeid fish is visible.C, D: Optical photograph of another paraclupeid (Poi-SGM 10) and SEM images (SE mode) of its finely phosphatized muscles (after Dutheil, 1999: figs. 5 & 6).E: SEM images (SE mode) of mineralized muscles from the penaeid shrimp Cretapenaeus berberus (MNHN.F.A24633) (after Garassino et al., 2006: fig. 5).F: Infrared spectrum of mineralized muscles from C. berberus.