Earth-Science Reviews 179 (2018) 95–122 Contents lists available at ScienceDirect Earth-Science Reviews journal homepage: www.elsevier.com/locate/earscirev Invited review Understanding biomineralization in the fossil record Alberto Pérez-Huerta a,b,⁎ c , Ismael Coronado , Thomas A. Hegna d T a Department of Geological Sciences, The University of Alabama, Tuscaloosa, AL 35487, USA Alabama Museum of Natural History, The University of Alabama, Tuscaloosa, AL 5487, USA Institute of Paleobiology, Twarda 51/55, 00-818 Warsaw, Poland d Department of Geology, Western Illinois University, Macomb, IL 61455, USA b c A B S T R A C T Biomineralization – the formation of minerals by organisms – is a key aspect in the understanding of the fossil record. Knowing how biominerals form and their properties is important in the correct use of fossils in geochemistry, the understanding of evolution, and in the interpretation of how geological events have influenced the fossil record throughout the Phanerozoic. The focus of this contribution, rather than a conventional review on the status of this research field, is on the importance of highlighting the traditional link between paleontology and biomineralization. 1. Introduction Biomineralization can be defined as a set of processes by which organisms form minerals (Weiner and Dove, 2003). In biologicallycontrolled mineralization, biominerals are primarily composites of two constituents, a mineral phase(s) and an organic (multi-)component, in different proportions (Fig. 1). Because of the mineral constituent, it could be argued that geologists, such as Ove B. Bøggild and James S. Bowerbank, pioneered the modern study of biomineralization in the 19th century (see Cuif et al., 2011). This early work led to studies establishing a parallel between the formation of biominerals and their abiogenic counterparts. This resulted in the application of biominerals for the reconstruction of past environmental conditions (Urey et al., 1951). As a result of this line of inquiry, geologists favored the use of fossils for climate reconstruction and in the process overlooked the importance of biology in biomineral formation. One prominent exception to this kind of oversight was Heinz A. Lowenstam who began investigating biominerals and their formation in the 1960s (Weiner, 2008) and thus, became a crucial figure in highlighting the significance, and multi-disciplinary nature, of biomineralization research. In addition, the vast representation of mineralized structures in the fossil record led other paleontologists (Kenneth M. Towe, Harry Mutvei, Euan N. K. Clarkson, Jean Pierre Cuif, among others) to recognize broader connections between biomineralization and paleontology, beyond simply the application of fossils in paleoclimatology. Even though this field began with geologists more than a century ago, in the last 40 years, the study of biominerals has been overtaken by physicists, engineers, and (bio-)chemists to develop novel biomaterials and to apply biomineralization studies in medicine. Yet, several geologists, most of whom have a paleontological background (see Acknowledgements), are currently making important contributions to the field of biomineralization. New approaches to biomineralization research, in addition to the development of novel techniques such as atomic force microscopy (AFM), can contribute to a better understanding of the fossil record. Also, the study of fossils can impact the knowledge of biominerals produced by extant organisms. The aim of this review is, therefore, threefold as follows: i) to introduce the latest developments in biomineralization research to the geoscience community; ii) to illustrate how the knowledge of biomineralization is important for interpreting the fossil record; and iii) to discuss potential areas of research at the intersection of paleontology and biomineralization. 2. Biomineral characteristics The diversity of biominerals is at least as high as taxa that have the ability to biologically control mineralization. The number of described mineralized structures and chemical compositions of the mineral phase, Abbreviations: ACC, amorphous calcium carbonate; AFM, atomic force microscopy; APT, atom probe tomography; CIP, computer-integrated polarization; CL, cathodoluminescence; EBSD, electron-backscatter diffraction; FEG-SEM, field-emission secondary electron microscopy; FTIR, Fourier-transform infrared spectroscopy; HMC, high magnesium calcite; IOM, intercrystalline organic matrix; LMC, Low Magnesium Calcite; RAD, Rapid Accretion Deposits; SEM, Scanning Electron Microscopy; SOM, Soluble Organic Matrix; TD, Thickening Deposits; TEM, transmission electron microscopy; XANES, X-ray absorption near edge structure spectroscopy; XRD, X-ray diffraction ⁎ Corresponding author at: Department of Geological Sciences, The University of Alabama, Tuscaloosa, AL 35487, USA. E-mail address: aphuerta@ua.edu (A. Pérez-Huerta). https://doi.org/10.1016/j.earscirev.2018.02.015 Received 29 September 2017; Received in revised form 16 February 2018; Accepted 16 February 2018 Available online 21 February 2018 0012-8252/ © 2018 Elsevier B.V. All rights reserved. Earth-Science Reviews 179 (2018) 95–122 A. Pérez-Huerta et al. Fig. 1. Example of biominerals. A. Image of a shell cross section of the brachiopod Hemithyris psittacea [scale bar = 5 mm]. B. Juvenile pearl oyster [scale bar = 500 μm; specimen courtesy of Jean Pierre Cuif]. C. Sea bass otolith [scale bar = 0.5 cm]. D. Zebra fish fin rays [scale bar = 0.5 mm; image adapted from Fig. 1 in Mahamid et al., 2008]. up by fibers (Fig. 2C; Cusack et al., 2008a, 2010). Optically, these fibers behave as continuous, single calcite crystals, with the c-axis perpendicular to direction of growth, but have a degree of flexibility that is absent in abiogenic calcite. In fact, the puncta shape is defined by the twisted morphology of calcitic fibers (Fig. 2B). At nanoscale level, proteinaceous sheets define the fiber morphology and triangularshaped structures are observed inside fibers caused by the interaction of the fiber's organic and mineral components (Cusack et al., 2008a). Yet, a detailed observation of fibers by atomic force microscopy (AFM) reveals that the basic components are rounded nanogranules with perfect alignment in relation to the fiber morphology (Fig. 2D; Pérez-Huerta et al., 2013a). The combination of all these structural elements provides the morphology and remarkable mechanical properties of brachiopod shells. A more complex example of hierarchical organization is well-illustrated in the case of siliceous hexactinellid sponges (see Weaver et al., 2007). The skeleton of the sponge Euplectella is hierarchically-constructed to withstand hydrostatic pressure and predation in deep-water environments (Aizenberg et al., 2005). Meanwhile, the same structural components provide optical properties to the skeleton of some species (i.e., E. aspergillum; Aizenberg et al., 2004) that could have biological significance for photoreception. Both brachiopods and siliceous sponges are just a couple of examples to demonstrate the hierarchical nature common to many biominerals produced by eukaryotes. as well as biomineralizing organisms, has increased since the first compilation by Lowenstam and Weiner in 1989. Yet, the basic biological principles governing biomineralization are highly conserved and the result of long- term evolutionary processes. As a consequence, a logical expectation is that biominerals, independently of taxon-specific biomineralization, should share some common characteristics (Mann, 2001). Recognizing these traits is then fundamental to understanding biomineralization in modern taxa and its importance in the fossil record. The last 30 years of biomineralization research have shown that, in general, biominerals are unique minerals based on five characteristics that can be enumerated as: 1) hierarchical organization; 2) biocomposite nature; 3) unique mineralization mechanisms; 4) biological crystallographic control; and 5) common nanostructure organization. 2.1. Hierarchical organization Biominerals are regarded as structures that self-assembly in several hierarchical levels, from nano- to macroscale (see for example Beniash, 2011). This organization confers biominerals a high level of structural complexity that is arguably one of their most recognizable and striking features in comparison with abiogenic counterparts. For example, a sea urchin spine is a unique and remarkable three-dimensional structure (e.g., Politi et al., 2004; Moureaux et al., 2010; Kelm et al., 2012). Even some biominerals that form inside vesicles (e.g., coccoliths) reflect the same level of structural complexity (Taylor et al., 2007). The resulting hierarchical organization of biominerals provides them with unique material properties for adaptation to the environment. A simple example to illustrate the hierarchical organization of biominerals can be found in the calcareous shell of a rhynchonelliform brachiopod (Fig. 2). Shells of Terebratulina retusa and Terebratalia transversa are composed of two layers, primary (outer) and secondary (inner), that are perforated by tubular structures termed “punctae” (Fig. 2A–B; Pérez-Huerta et al., 2009). At micron scale, the primary layer is composed by crystallites of calcite, with c-axis oriented perpendicular to the outer shell surface, while the secondary layer is built 2.2. Biocomposite nature Although biominerals ‘meet the criteria for being true minerals’ (Weiner and Dove, 2003; p. 7), biomineralization is quite unique and different to inorganic mineralization. One of the aspects that differentiate biominerals from their abiogenic counterparts is that biominerals are composites of mineral and organic phases (Lowenstam and Weiner, 1989). The organic content of biominerals is very variable (0– > 50 wt%) and depends upon the formation, type, and functionality of each biomineralized structure. In bone, for example, the organic 96 Earth-Science Reviews 179 (2018) 95–122 A. Pérez-Huerta et al. Fig. 2. Hierarchical organization in the shell of the brachiopod Terebratalia transversa. A. Synchrotron tomography image of the punctae, perforating the anterior shell region of the dorsal valve (red square; insert) [scale bar = 50 μm; more details in Pérez-Huerta et al., 2009]. B. SEM image of the shell interior showing the secondary layer fibers, and the formation of the punctae by the fibers [scale bar = 50 μm]; C. SEM of a shell cross section showing the primary (PL) and secondary layers (SL), with fibers, perforated by punctae [scale bar = 50 μm]. D. AFM image of the fibers, showing the protein encasing, and the nanostructure composed of rounded granules [scale bar = 50 μm; more details in Pérez-Huerta et al., 2013a]. the in situ characterization of the inter-crystalline organic matrices by X-ray absorption near edge structure spectroscopy (XANES) indicates differences among taxa (e.g., Cuif et al., 2003; Cusack et al., 2008b), despite the fact that sulfated sugars are a commonality for invertebrates secreting CaCO3 (Fig. 4; Cuif et al., 2011). These findings indicate that taxa across different phyla exert a specific control on the chemistry of their biomineral organic matrices. Further evidence of biological control on the IOM functional morphology has been shown recently. Checa et al. (2017) have demonstrated that the inter-crystalline organic matrix does not just serve as a scaffold for mineral growth but also plays an active role in the control of crystallography (Fig. 5; see also Section 2.3). The intra-crystalline organic matrix has been less studied, and its importance even neglected until the recent application of transmission electron microscopy (TEM) and AFM. In general, the intra-crystalline organic phase has been regarded as a “remnant” of mineral nucleation and growth, occluded in biomineral structures and with no functional role. However, Li et al. (2009) suggested a high-level of complexity for the arrangement of the intra-crystalline organic fraction and, more recently, its role in the mechanical properties of crystals has been shown (Kim et al., 2016). Moreover, the latest characterization of the chemical composition of the intra-crystalline organics, mainly by atom probe tomography (APT) (e.g., Gordon and Joester, 2011), reinforces their functionality. These findings point out that mineralizing organisms also control the chemical composition and arrangement of the intra-crystalline organic matrix, as they do with the inter-crystalline fraction. content varies between different types of bone and their mechanical roles (see Weiner and Wagner, 1998 and references therein). Overall, the organic content of phosphate-based biominerals secreted by vertebrates is higher than those built from carbonate or silica by invertebrates. Yet, the precise non-mineral (water and organic) content for most biominerals has not been determined. Focusing on biominerals produced by invertebrates, in particular those with carbonate compositions, two main organic components have been described: an inter-crystalline fraction present in-between structures; and an intra-crystalline fraction, inside the mineralized structure (i.e., a prism or nacre tablet). Until recently, the main component “recognized” in biomineralization research was the inter-crystalline organic matrix (IOM) because of the relatively ease with which it can be visualized through microscopic techniques (Fig. 3). Structural characterization of carbonate biominerals indicates that IOM serves as a template for mineral nucleation and/or a scaffold for mineral growth and emplacement (see Cuif et al., 2011, 2012). IOM also plays a key role in determining the final morphology of crystalline units, as in the case of calcitic prisms in bivalve shells (Figs. 3–5). Recently, the degree of biological influence over the functionality of IOM has been questioned (Bayerlein et al., 2014). However, the chemical composition of these organic matrices and the relationship mineral-IOM strongly argue in favor of such biological control. The analysis of insoluble organic matrices reveals differences among organisms, even within the same phylum (Fig. 6), despite the common presence of proteins, polysaccharides and lipids (e.g., Dauphin, 2001a; Farre et al., 2010). Also, 97 Earth-Science Reviews 179 (2018) 95–122 A. Pérez-Huerta et al. et al., 2010). Nevertheless, not all structures form via controlled-mineralization use amorphous precursors, such as bacterial magnetite and oyster shells of Crassostrea nippona (see Weiner et al., 2009; Kudo et al., 2010). Yet, examples of organisms that do not employ amorphous precursor phases seem to be rare. By definition, amorphous precursor phases are unstable and rapidly transform into a crystalline phase, which has generated difficulties for their study in biomineralization (see De Yoreo et al., 2015). However, some organisms have mastered the ability to keep these amorphous phases stable for physiological purposes. For example, some arthropods store ACC nanoparticles in gastroliths as a fast source of calcium for mineralizing their exoskeleton after molting. Stable ACC has been also found in the glands of earthworms (e.g., Gago-Duport et al., 2008) and the intestinal tracts of fish (Foran et al., 2013) as a way to regulate whole body calcium homeostasis. Mineralizing organisms tend to use two major strategies to stabilize ACC: either by using specific organic macromolecules (mainly proteins) or unusually high concentrations of magnesium, or a combination of both (e.g., Addadi et al., 2003). The involvement of amorphous phases in biomineralization, either in in a stable form or as transient phase for mineralization, is a widespread mechanism. This strategy appears to be a unifying principle for mineralizing organisms and, probably, “evolved in a common ancestor of the Bilateria animals” (Weiner et al., 2009, p. 107). 2.4. Biological crystallographic control Mineral-producing organisms exert precise control on the crystallographic orientation of biomineral structures (Pérez-Huerta and Cusack, 2008). Independent of the level of biomineral complexity, organisms retain the ability to determine preferred crystallographic orientations. As with the hierarchical organization, such crystallographic control is mainly aimed to enhance the mechanical properties of biominerals (e.g., Fratzl and Weinkamer, 2007; Meyers et al., 2008). Also, specific orientations of optical axes of crystals improve functional morphology as in the case of photoreception (see Section 6). The degree of crystallographic control varies among organisms but, in particular, it depends on the scale of observation. The precise orientation of crystallographic axes is different when considering a single biomineral unit (i.e., calcite prism) rather than a polycrystalline layer (i.e., palisade layer of an eggshell). The aforementioned sea urchin spine behaves optically as a single calcite crystal with c-axis perfectly aligned with the growth axis of the spine (Fig. 9A–B; Moureaux et al., 2010). The overall analysis of the crystallographic orientation of nacreous layer in a mussel shell reveals the aragonite c-axis perpendicular to the nacreous laminae and the outer surface of the shell (Fig. 9C–D; England et al., 2007). Yet, the orientation of a- and b-axes of aragonite of nacre tablets within the nacreous layer is less constrained (Fig. 9D) and it could be attributed to the screw dislocation model for the growth of nacre (see Dalbeck et al., 2006). The crystallographic control exerted by organisms during mineralization is a defining characteristic of biominerals that is manifested exceptionally well in fossils (Fig. 10). In fact, crystallographic criteria can be used to identify primary biogenic structures in the fossil record (see Section 3) and the effects of diagenesis (see Section 5). Well-preserved fossilized biomineral structures present preferred crystallographic orientations that relate to the architecture of the biomineral structure and its functional morphology (Coronado et al., 2013). Also, the crystallographic control attained by extinct taxa frequently matches that of Recent organisms allowing the reconstruction of the original morphology of biomineralized structural components. For example, Coronado et al. (2015a) showed that 3D structural elements (i.e., spines) of Carboniferous coral skeletons can be reconstructed from 2D fossil sections based on crystallographic characteristics (Fig. 10A). Furthermore, the mechanisms for the biological crystallographic control seem to be conserved and with deep evolutionary roots. Following with the example of nacre (Fig. 9), molluscs have produced shells with Fig. 3. Example of inter-crystalline organic matrix (IOM). A. Image of IOM, after mineral decalcification, from the nacreous layer of Mytilus edulis shell [scale bar = 1 μm]. B. Image of the IOM extracted from the shell of the fossil gastropod Ecphora [scale bar = 250 μm; image adapted from Fig. 2 in Nance et al., 2015]. 2.3. Unique mineralization mechanisms Non-classical crystallization pathways have emerged as an important component of mineralization in synthetic and natural systems (Fig. 7; De Yoreo et al., 2015). Mineralizing organisms, in general, use this strategy for the formation of biominerals, rather than precipitating them from a saturated ionic solution. Among the non-classical crystallization mechanisms, biomineralization has been shown to commonly occur via the formation of precursor amorphous phases (see Weiner et al., 2009 and references therein). The idea of amorphous phases linked to biomineralization was already hinted at in older literature (see references in Fratzl and Weiner, 2010), but the concept did not receive full attention until the analysis of biomineralization in chiton teeth (Towe and Lowenstam, 1967; see also Weiner, 2008). Amorphous calcium carbonate (ACC) is the best-studied case of amorphous precursor phases in biomineralization, after the pioneering work of Beniash et al. (1997) in sea urchin larval spicules. This work was followed by the demonstration that ACC plays a role in carbonate biomineralization even in fully mature structures (Fig. 8; see Politi et al., 2004). Currently, the involvement of ACC is accepted as a “quasi-universal” precursor phase in carbonate biomineralization (see Addadi et al., 2003; Cusack and Freer, 2008; Weiner et al., 2009; Gal et al., 2015). Following the research on ACC, the importance of amorphous phases was also highlighted for phosphate biomineralization. Amorphous calcium phosphate (ACP) is a major precursor phase in the formation of bone (Fig. 8; e.g., Mahamid et al., 2008, 2010; Nudelman 98 Earth-Science Reviews 179 (2018) 95–122 A. Pérez-Huerta et al. Fig. 4. Example of in situ imaging (SEM) and characterization (XANES mapping) of the IOM in mollusc shells; arrows indicate examples of the location of organic components, which are enriched in sulfated polysaccharides as shown by higher concentration (red-orange) on the sulfur (S) map [images replicated from Fig. 2 in Cuif et al., 2012]. Fig. 5. Example of in situ characterization, by SEM and EBSD [with colors indicating different crystallographic planes of calcite and dark regions no diffraction related to the presence of organics], of organic matrices (arrows) and calcitic prisms from a bivalve shell [scale bars = 20 μm (left image) and 10 μm (right image); images adapted from Fig. 2 in Checa et al., 2017]. 99 Earth-Science Reviews 179 (2018) 95–122 A. Pérez-Huerta et al. and aragonitic biominerals within the Phylum Mollusca (Dauphin, 2008). Most recent research has provided evidence of the presence of similar nanogranules in biominerals of taxa across different phyla, including brachiopods, corals, sponges, and arthropods (Fig. 11; Cuif et al., 2011; Gal et al., 2015). AFM observations have further suggested that the nanogranules are composites of a mineral phase surrounded by a cortex potentially composed of a combination of organics and amorphous phase (i.e., ACC) (Fig. 12). Nanogranules are not found in all biominerals (see Gal et al., 2015), but are ubiquitous among the calcareous biominerals secreted by invertebrates (Cuif et al., 2011). Furthermore, a similar nanogranular organization of biominerals can be found in the fossil structures of corals (Coronado et al., 2013), molluscs (see Cuif et al., 2011), and brachiopods (Pérez-Huerta, pers. obs.) (Fig. 12). The importance of nanogranules, as the basic building blocks in many biominerals, has only recently been recognized, and it deserves further research. Nevertheless, this finding has led to the hypothesis that, in some cases, biomineralization can be the result of growth by nanosphere particle accretion, and that the nanospheres are preserved upon crystallization (see Gal et al., 2015). 3. Recognizing primary biomineral structures in fossils Well-preserved fossil mineral skeletons (e.g., shells, bones, teeth, carapaces, eggs, spicules, etc.) are a key in the study and subsequent interpretation of the fossil record (e.g., Knoll, 2003; Wood and Zhuravlev, 2012). The origin and processes of formation of mineralized structures inform us about the evolution of life as well as the interpretation of geological events (i.e., mass extinctions) throughout Earth's history. Thus, distinguishing the primary, distinctive properties of fossil biominerals, as opposed to diagenetically imposed properties, is of paramount importance for understanding the significance of biominerals in a paleontological context. The presence of any of the shared characteristics of biominerals should be a starting point to recognizing primary, biogenic structures in fossils (see Section 2 and also Mann, 2001). The task is not straightforward because of the difficulty in detecting the presence of organics and precursor phases for crystallization in fossils. Also, diagenesis can have a major impact on the structural composition of fossil biominerals, including the hierarchical organization and their nanostructure (see Section 5). However, in this section, three aspects are evaluated with the purpose of discerning the primary nature of biomineralized structures in fossils: 1) identification of the original mineralogy, 2) analysis of fine-scale structures that form skeletons, and 3) identification of selfassembled structures. Fig. 6. Example of FTIR analysis of organic matrices from decalcified coral skeletons; grey bars indicate areas of comparison for differences in lipid and sugar contents [figure replicated from Fig. 6 in Farre et al., 2010]. nacreous structures with the same preferred crystallographic orientations at least since the Mesozoic (Fig. 10C–D). Recent research has suggested that there is a molecular level control on crystallographic control and preferred crystallographic orientations are already present at sub-micron level scale (see Mastropietro et al., 2017). Although the biological control on crystallography is a shared, trademark characteristic of biominerals, our knowledge of how organisms achieve it is still unknown. As such, this is one of the fundamental, long-standing unanswered questions in biomineralization (Towe, 1972, 2006). 3.1. Identification of the original mineralogy Fossils, resulting from biologically-controlled mineralization, are present in the marine and terrestrial realms, but their fossil record is discontinuous (Knoll, 2003). They are composed of different mineralogies (Lowenstam and Weiner, 1989); however, those composed of calcium carbonate (CaCO3) are the most ubiquitous and most broadly studied in Earth sciences due to their significance in paleoclimatic and paleoenvironmental reconstructions (e.g., Austin and James, 2008). The preservation of the original mineralogy in a fossil largely depends on whether the solubility threshold of a given mineral has been crossed during its diagenetic history (cf. Knoll, 2003). For example considering CaCO3, the highest degree of solubility is present in ACC, the most metastable form (especially in the hydrous form), and decreases in the three anhydrous polymorphs: vaterite, aragonite, and calcite. Calcite presents two forms depending on the magnesium content (Chave, 1954): high magnesium calcite (HMC, > 4 mol%) and low magnesium one (LMC, < 4 mol%). In addition, some authors distinguish a third form of calcite with a composition intermediate between HMC and LMC (Stanley et al., 2002; Ries, 2005). The magnesium content also modifies the solubility of the mineral phase and, in 2.5. Common nanostructure organization Advancements in the field of microscopy have traditionally resulted in major leaps in our understanding of biomineralization. Recent developments in field-emission secondary electron microscopy (FEG-SEM) and atomic force microscopy (AFM) have allowed the structural characterization of biominerals at nano- and microscales. At the nanoscale level of observation, a surprising discovery was that aragonitic biomineral units (i.e. nacreous tablets) in shells are composed of (sub-) rounded nanogranules (Dauphin, 2001b). Subsequent investigations have revealed that this nanostructure is characteristic of both calcitic 100 Earth-Science Reviews 179 (2018) 95–122 A. Pérez-Huerta et al. Fig. 7. Pathways to crystallization by attachment [figure replicated from Fig. 1 in De Yoreo et al., 2015]. trilobite cuticles (Dalingwater, 1973; Teigler and Towe, 1975), calcitic scleractinian corals (Stolarski et al., 2007), aragonitic belemnites (Dauphin et al., 2007), aragonitic phylloid algae (Kirkland et al., 1993), and serpulid worm tubes (Vinn et al., 2008). Raman and Fouriertransform infrared (FTIR) spectroscopy techniques have been applied to aragonitic brachiopods (Balthasar et al., 2011), Triassic scleractinian corals (Frankowiak et al., 2013), and aragonitic molluscs (Faylona et al., 2011). Finally, electron backscatter diffraction (EBSD) has been used in the analysis of LMC in Paleozoic corals (Coronado et al., 2013, 2015a), brachiopods (Pérez-Huerta et al., 2007b; Cummings et al., 2014), molluscs (Harper and Checa, 2017), dinosaur eggshells (GrelletTinner et al., 2011; Eagle et al., 2015; Moreno-Azanza et al., 2013, 2017), LMC-HMC lenses of trilobites (Lee et al., 2007; Lee et al., 2012; Torney et al., 2014), and also in aragonitic remains in brachiopods (Balthasar et al., 2011) and scleractinian corals (Janiszewska et al., 2015). descending order of solubility, we can organize the decreasing solubility of calcium carbonate minerals as ACC > vaterite > HMC > aragonite > LMC. Porter (2010, p. 259–261) summarized and discussed the classical criteria used in the literature for determining the primary carbonate mineralogy of fossil biominerals, although similar principles could be used for other mineralogies as well. The criteria are as follows: 1a) part or whole of fossil preserved as aragonite; 1b) comparison with co-occurring aragonite fossils at the same locality; 2) phylogenetic inference based on mineralogy of younger members of the taxon; 3) quality of preservation of original microstructures in calcite; 4) secondarily replicated microstructures and crystal morphologies (e.g., phosphatization, silicification) in oldest rocks and sediments; 5) trace element chemistry. Once the criteria are established, several crystallographic and spectroscopic techniques are often used to characterize the primary mineralogy present in fossils. X-ray diffraction has been used in calcitic Fig. 8. Example of amorphous phases involved in the biomineralization of a sea urchin spine [left; figure replicated from Fig. 1 in Politi et al., 2004; A–E indicate the sequence of sea urchin spine crystallization, from a fully, formed mature spine in A to incipient spine with amorphous (ACC) in E] and zebra fish fin rays [right; red arrows – fully crystalline/white arrows – amorphous; figure modified from Fig. 1 in Mahamid et al., 2008]. 101 Earth-Science Reviews 179 (2018) 95–122 A. Pérez-Huerta et al. Fig. 9. Example of biological control on crystallographic attributes of Recent biominerals. A. Synchrotron tomography reconstruction of a cross section of a sea urchin spine [scale bar = 5 μm]. B. EBSD map of a cross section of a sea urchin spine, showing the c-axis of calcite perpendicular to the cross section [scale bar = 500 μm; more details in Moureaux et al., 2010]. C. SEM image of a portion of the nacreous layer in the shell of Mytilus californianus [scale bar = 5 μm]. D. EBSD map on the same region as C, showing the c-axis of aragonite (white arrow) perpendicular to the thickness of nacre tablets [scale bar = 10 μm]. The presence of ACC or vaterite has not been demonstrated in the fossil record yet due to their metastability (higher in aqueous conditions; see Spann et al., 2010). However, the transformation from vaterite to calcite has been shown for those biominerals originally formed by vaterite, as in the case of some Miocene statoliths of crustaceans of the family Mysidae (see Wittmann et al., 1993). Skeletons composed of aragonite and/or high-Mg calcite are comparatively scarce in the fossil record (Hall and Kennedy, 1967; Dickson, 2002; Stolarski et al., 2009; Gorzelak et al., 2016). Both mineralogies are metastable at Earth's surface conditions (Morse and Mackenzie, 1990), and both aragonite and high-Mg calcite transform quickly to low-Mg calcite in aqueous solutions and by solid-state transformation (Land, 1967; Bischoff, 1969; Perdikouri et al., 2011; Casella, 2017). However, it is worth highlighting some discoveries in this regard. The oldest remnants of original aragonite are reported in fossil brachiopod shells from Ordovician and Silurian rocks (Balthasar et al., 2011). This is an exceptional discovery due to the rare and irregular aragonitic fossil record in Paleozoic, mainly consisting of some molluscs and algae (e.g., Stehli, 1956; Hallam and O'Hara, 1962; Brand, 1989; Kirkland et al., 1993; Seuß et al., 2009). Also, the presence of original aragonite has been hinted at for other fossils based on relics or molds of certain microstructures (e.g., Sandberg and Hudson, 1983; Maliva and Dickson, 1992; Wendt, 1989). Thus, the finding of aragonitic fossils is considered a sign of original mineralogy and pristine preservation. Nevertheless, secondary precipitation of aragonite, by overgrowth or infilling processes, can readily affect calcium carbonate biominerals shortly after burial and in the first stages of diagenesis (Hendry et al., 1995; Webb et al., 2007; Frankowiak et al., 2013; Gothmann et al., 2015). Such secondary-precipitation processes are promoted by high Mg:Ca ratio of marine that stabilize the aragonite precipitation (Fernandez-Diaz et al., 1996). The presence of secondary aragonite can be detected by modifications of geochemical markers rather than by mineralogical changes (Dauphin et al., 1996; Dauphin et al., 2007; Frankowiak et al., 2013; Gothmann et al., 2015). 3.2. Analysis of fine-scale structures Each group of mineralizing organisms shows different crystal shapes, sizes and distributions (i.e., textures) in their skeletons, grouped in crystalline domains that define biomineral structural units (e.g., nacre tablets, crossed lamellar, prisms, fibers). The microstructure (sensu Checa et al., 2011) of each calcifying organism may be composed of crystals having a single or multiple mineralogies (e.g., Lowenstam and Weiner, 1989) and different crystal morphologies and arrangements (Fig. 13B–D). Many microstructural studies of calcified skeletons, including fossils, of cnidarians (e.g., Wang, 1950; Lafuste and Plusquellec, 1985), coralline sponges (Wendt, 1990), molluscs (Carter, 1990), brachiopods (Williams, 1968; Williams et al., 1998), and annelids (Vinn, 2007) have a primarily taxonomic purpose. This effort to establish a systematic analysis of crystal habits, sizes, and textural relations in the context of taxonomy is considered a powerful approach to detect primary biological mineralized structures (e.g., Sandberg, 1975; Rodríguez, 1989). The most common microstructural criterion to establish the primary nature of a biomineral structure (e.g., Rodríguez, 1989; Porter, 2010) is based on the regularity of these microstructures in fossils within specific taxa classified within the same “taxonomic domain”, such as Phylum or Family. Another useful criterion is the presence of the same microstructures in related taxa of different age (e.g., in the Paleozoic and Recent), or the presence of the same microstructure in different diagenetic environments and stages of preservation (see Rodríguez, 1989; Stolarski, 2000). Finally, additional evidence of the primary nature of a biomineral structure is gained when an organism repairs their skeletons during its life using the same microstructural elements (Falces, 1997). Even though these criteria are robust, the microstructural replication, or even partial replication, during diagenesis has been widely documented in the transformation of aragonite to calcite in molluscs (Sandberg and Hudson, 1983; Maliva and Dickson, 1992) and scleractinian corals (Stolarski, 2000; Frankowiak et al., 2013). Also, this 102 Earth-Science Reviews 179 (2018) 95–122 A. Pérez-Huerta et al. beyond the micro-scale to the nano-scale and has advanced the knowledge of processes leading to preservation of primary structures (see Section 5). 3.3. Identification of self-assembled structures Biominerals are hierarchical organo-mineral composites of crystalline units with different shapes, sizes, and distributions from micro- to nanostructural scales of observation (see Section 2). The assessment of this organization provides information about the relationships between diverse elements (at macro- and micro-scales; Pérez-Huerta et al., 2013a), processes of crystal growth (Sun et al., 2017), and the architectural responses to eco-phenotypic variations (Fitzer et al., 2016). Yet, the finding of self-assembled structures is also key to the identification of primary structures in fossils. The hierarchical structure of fossil skeletons can be observed at different scales, and good examples are structural elements, such as septa and tabulae in corals, the hinge mechanism of brachiopod shells, or teeth in sea urchins (see Cuif et al., 2011). The best examples of how to analyze and describe hierarchically-organized structures in the fossil record are from the analysis of Phanerozoic corals (e.g., Stolarski et al., 2007, 2016; Cuif et al., 2011; Coronado et al., 2013, 2015b, 2016; Fig. 13). The assumption of the presence or absence of the original mineralogy, however, is by itself insufficient to ensure identification of primary biomineral structures in fossils (e.g., Dauphin et al., 1996; Dauphin, 2002; Stolarski et al., 2007; Balthasar et al., 2011). Also, neither the presence of preserved fine-scale structures nor hierarchically-organized structures are sufficient by themselves. Yet, the combination of these criteria, plus others related to the nanostructure and crystallographic arrangements of the microstructure (see Section 5), are solid clues for identifying pristine biominerals in the fossil record. 4. Fossil biominerals and organics Paleontologists are typically restricted to looking at only the mineral phase of biomineralized skeletons and shells. It is the most obvious part of fossil remains, sometimes the only part that is left. More importantly, however, it is the role played by the organic phase(s) (see Section 2.2). The organic framework is postulated to have several roles for the organism during biomineralization. In general, it participates in mineral nucleation, determines the mineral phase deposited (i.e., calcite vs. aragonite), and controls the crystallographic orientation and growth of the incipient mineral crystals (Crenshaw, 1990). Exceptional fossil preservation can lead to the in situ observation of the inter-crystalline organic matrix (Fig. 3; Nance et al., 2015), although examples are scarce. Nevertheless, some evidence of “relic” organic matrix in well-preserved microstructures is described in carbonate fossils throughout the geological record. Examples of organic remnants have been described inside crystals (i.e., nacre tablets in ammonoids; Dauphin, 2002; Cuif et al., 2011), around crystals in trilobite cuticles (Teigler and Towe, 1975; Dalingwater and Miller, 1977), as well as in brachiopod (Garbelli et al., 2012; Riechelmann et al., 2016) and bivalve (Dreier et al., 2014) shells. Also, traces of organics have been found in specialized structures of skeletons (i.e., Rapid Accretion Deposits (RAD) in scleractinian corals; Stolarski, 2003; Stolarski et al., 2007), growth lines in belemnite rostra (e.g., Sælen, 1989; Benito and Reolid, 2012; Stevens et al., 2017), and exocuticle in trilobites (Mutvei, 1981).These findings have been used as a further evidence to support the presence of primary mineralized structures in fossil skeletons (see Section 3). From a paleontological perspective, a more interesting idea is whether these organic matrices can increase the preservation potential of originally weakly mineralized structures. This is the case of certain groups within the Phylum Arthropoda, which has a significant presence in the fossil record (see Edgecombe, 2010). In many arthropods, the Fig. 10. Example of biological control on crystallographic attributes of fossil biominerals. A. 3D reconstruction of a coral spine based on EBSD data [scale bar = 100 μm; see more details in Coronado et al., 2015a]. B. SEM image of columnar nacre in the shell of Cretaceous ammonoid, indicating the orientation of the aragonite c-axis in sections perpendicular and parallel to the outer shell surface (red arrow) [scale bar = 10 μm]. C. EBSD map of the section parallel to the outer shell surface (red arrow on B), showing red color representing the aragonite c-axis parallel to map view and black areas of no diffraction due to porosity and remnants of inter-crystalline organic matrix [scale bar = 20 μm]. replication can occur during recrystallization of LMC calcite structures as reported in brachiopods (Cusack and Williams, 2001; Garbelli et al., 2012) and Paleozoic corals (Coronado and Rodríguez, 2016). The application of uniformitarianism, in the study of fossil biominerals, has allowed modification of the scale of observation of fossil skeletons 103 Earth-Science Reviews 179 (2018) 95–122 A. Pérez-Huerta et al. Fig. 11. SEM images illustrating the granular nanostructure in biominerals. A, E. An isolated calcitic prism of the bivalve Atrina rigida; B, F. Fracture in the nacreous layer of the shell of the cephalopod Nautilus pompilius showing the aragonitic tablets. C, G. Asymmetric triradiate spicule from the calcareous sponge Sycon sp. D, H. Skeletal part (calcitic) from the brittle star Ophiocoma wendtii [figure replicated from Fig. 2 in Gal et al., 2015]. strengthen and reinforce it (e.g., Dudich, 1931; Becker et al., 2005). These biomineralized structures can be identified as: 1) spherules (20–50 nm diameter) augmenting individual nanofibrils of chitin, 2) mineral tubes enclosing the nanofibrils, 3) mineral tubes enclosing bundles of these nanofibrils (chitin-protein fibers), or 4) a solid mineral matrix surrounding the bundles of chitin-protein fibers (Fig. 14; Fabritius et al., 2016). This chitinous extracellular matrix appears to organic framework does not get only involved in mineral nucleation and growth but also serves a vital structural role (Fabritius et al., 2016). This organic framework is made up of a polysaccharide named chitin, which is hierarchically organized in fibers that form sheets and sheets that are piled together in a “twisted plywood” structure (Fig. 14; Raabe et al., 2005; Fabritius et al., 2016). Particularly in crustaceans, this organic framework is augmented with biomineral structures that 104 Earth-Science Reviews 179 (2018) 95–122 A. Pérez-Huerta et al. Fig. 12. AFM images illustrating the nanostructure in the fossil coral Calceola sandalina. A. Amplitude image showing the overall nanogranular texture. B. Phase image where the pill-shaped nanotexture can be observed in a transverse section of a microcrystal; note the dark envelopes around nanocrystals (white arrow) [figure modified and adapted from Fig. 4 in Coronado et al., 2016]. control the deposition of calcium carbonate by itself in crustaceans in contrast to an underlying cell layer (Dillaman et al., 2013). However, rather than being localized to where minerals are deposited, such matrix forms the entire body (exoskeleton) covering arthropods. Arthropods have several options for hardening their chitinous exoskeletons, with biomineralized structures being but one strategy Fig. 13. Primary structural characteristics of a transversal section of a Palezoic coral (Tabulata) Multithecopora sp. D (Coronado et al., 2015b) from the Valdeteja – Las Majadas section (Valdeteja Formation, León, Spain, of mid-Bashkirian – early Moscovian age, Upper Carboniferous). A. Cathodoluminescence image of coral skeleton (NL: non-luminescent calcite; SL: Slightly-luminescent calcite; L: Luminescent calcite). Note that the L zones correspond with the external and inner fibrous domains of microstructure, which are luminescent, whereas the inner zones of skeleton are non-luminescent. B. Ultrathin-section image that shows a detail of the contact between the lamellar domain and inner fibrous domain (F: fibrous domain; L: lamellar domain). C. SEM image showing a transversal cross section of a Multithecorpora and details of the two domains showed in the (B) image. D. Natural breakage of lamellae, showing the sub-microlaminae that form the microcrystals (white arrow). E–J. AFM images showing the nanostructural features of Multithecopora. Height images of lamellae (F) and fibers (E) showing the inner structuration forming sub-microlaminae, black-square on (E) refers to images (I–J). G. Phase image of the (E) image where can be observed that microcrystals are formed by aggregation granular nanocrystals. H. Composed image of height, amplitude and phase showing a detail of dark envelopes that surround the nanocrystals (white arrow points to the relief of envelope). I–J. Height and phase images showing the contact between to microcrystals the presence of mineral bridges (white arrow) and the formation of submicrolaminae. K) Three dimensional AFM image of nanogranules of Multithecopora, showing the co-orientation of them-self and a roughness analysis of the sample. Note the high topography in comparison with the analysis showed in the Fig. 15. 105 Earth-Science Reviews 179 (2018) 95–122 A. Pérez-Huerta et al. Fig. 14. Schematic of the arrangement of the mineralchitin framework in the exoskeleton of arthropods. Nanofibrils can be decorated with spherical particles (1) or enclosed by mineral tubes (2), which was also observed for larger chitin-protein fibers (3). In some cases, clusters of nanofibrils occur embedded in a solid mineral matrix (4) [figure modified and adapted from Fig. 1 in Fabritius et al., 2016]. molecular signature of a chitin-protein complex has been found in Silurian-aged eurypterid cuticle (Cody et al., 2011). The importance of organics phases in biomineralization is wellknown, but the case of arthropods also demonstrates their significance in shaping the fossil record of mineralizing organisms. New technique developments, such as fluorescence microscopy, with or without organic staining (Gautret, 2000; Stolarski, 2003; Dreier et al., 2014; Benito et al., 2016; Hoffmann et al., 2016), are increasing our capacity to detect organic phases in fossils. This information is fundamental for a better understanding of the geological record of biomineralization. However, caution should be exercised as organic impurities of crystals could have a secondary origin related to early diagenetic processes (see for example Coronado et al., 2016). utilized mostly by crustaceans. In crustaceans, certain portions, or sclerites, of the exoskeleton are selectively mineralized for hardness, while other regions are left pliable (i.e. joint regions; Ruangchai et al., 2013). Crustaceans exhibit a high degree of control over the amount of mineralization that occurs, with structures like claws being heavily mineralized (Waugh et al., 2006). Other regions, such as eyes, exhibit an entirely different pattern of mineralization and a chitin structure than the head region (Alagboso et al., 2014). This demonstrates a fine spatial biological control on the cuticle differentiation. The functional advantages of the arthropod exoskeleton come at a cost. Unlike molluscs and brachiopods, which grow by marginal accretion, and vertebrates, which are able to extensively remodel their internal skeleton, arthropods must molt in order to grow. This process requires that the animal shed its old exoskeleton in order to grow larger while simultaneously growing a new, larger exoskeleton underneath its old one. Rather than wastefully discarding their old exoskeleton, many crustaceans resorb the mineral content prior to molting (sometimes only a particular mineral phase, see Neues et al., 2011) and later consume their shed exoskeleton after molting. However, ostracods (Turpen and Angell, 1971) and trilobites (Miller and Clarkson, 1980; Mutvei, 1981) are important exceptions that do not appear to resorb any minerals from their exoskeletons. The presence and importance of arthropods in the fossil record can be attributed to the nature, formation, and structural role of the exoskeleton. The mineral phase of the exoskeleton is much more durable than the organic phase (usually quickly degraded by bacteria), although relict microstructures of the chitin framework can be preserved. However, the eventual loss of the chitinous microstructure is not well understood, as it is the chemical evolution of the cuticle, during diagenesis. The organic phase is turned into an aliphatic polymer (nanoscale composite of waxes) that degrades to a nitrogen-rich, vestigial chitinprotein complex (Cody et al., 2011). What is remarkable is that this degraded, vestigial chitin-protein complex can be recovered via acid digestion with hydrofluoric acid, and its “microscopic anatomy” can be studied in rocks as old as the Cambrian (Harvey and Butterfield, 2008; Harvey and Pedder, 2013). Original chitin has only been detected in fossils as old as the Oligocene (Stankiewicz et al., 1997), but the 5. Biominerals and diagenesis Recognizing primary biogenic structures (see Section 3) and diagenesis are related topics, yet different in the context of analyzing biomineralization in the fossil record. The former is analyzed herein in relation to the latest knowledge of biomineralization research by linking modern biominerals to fossil counterparts using a uniformitarian, biological approach. Diagenesis, however, has been a main subject of study in Earth sciences for several decades. Fossil biominerals record biogeochemical signals from the surrounding environment (Urey et al., 1951), and those fossil skeletons that still preserve primary biomineral structures contribute to reconstruct past of Earth's climate and environments throughout the Phanerozoic. Diagenesis can compromise the quality of preservation for fossil skeletons and thus, the record of primary geochemical signals. Diagenesis has been defined as “all those changes that take place in sediment near the Earth's surface at low temperature and pressure and without crustal movement being directly involved” (Taylor, 1963, p. 884). Within this context, it is important to consider early diagenetic processes, eodiagenesis or biostratinomy (sensu Gastaldo, 2007), which refer to all processes occurring after the death of an organism until its initial burial (Fernández-López and Fernández-Jalvo, 2002) and even after shallow burial, such as disarticulation, dissolution, abrasion, 106 Earth-Science Reviews 179 (2018) 95–122 A. Pérez-Huerta et al. Fig. 15. Structural characteristics of a transversal section of a Palezoic coral (Tabulata) Multithecopora sp. D affected by silicification. The coral belongs to the same locality and age that those showed in the Fig. 13. A. Cathodoluminescence image of coral skeleton (SL: Slightly-luminescent calcite; L: Luminescent calcite). Note that the L zones correspond with the matrix and micro-fractures, whereas the inner zones of skeleton are slightly-luminescence in comparison with Fig. 13. The silicification area is NL, unless the contact zones with the calcitic skeleton, which are luminescence. B–D). SEM images showing a transversal cross-section of the coral and details of the lamellar domain predated by the silicification front (Cc: calcite; Si: silica). B) White arrow points to the front of silicification, which follow the contact area between microcrystals. C. Detail of a small silicification gulf where the preservation of calcitic microstructure still is evident but with signs of recrystallization and dissolution. D. Detail of an area where the original microstructure has been totally eroded and the silica present a euhedral shape (white arrow), in comparison with the rounded shape of images (B–C). E–L. AFM images of the silicification front: E–G. Height and phase images of the silicification front. Note the different colors in phase image (response of different viscoelastic properties) of silica, calcite and the contact area; H. Roughness analysis of the calcitic area, showing that the topography is more flat in comparison with figure Multithecopora; I–L. AFM images showing the nanostructural features of silicification area, note that the amorphous silica is subdivided in small micrometric crystals with curved boundaries percolating in the contact with the calcitic crystals (I–L); K–L. Phase image showing that the lamellae still exhibit some morphological remnants of submicrolaminae but the nanocrystals have loss the morphology, dark envelope and have reduce the size. production of ligands between hydroxyl groups and silicic, or polysilicic, acid promoting silicification (see Glover and Kidwell, 1993; Harper, 2000; Kidwell, 2005; Cuif et al., 2011). 4) The chemistry of the aqueous environment at the time of sedimentation (i.e., pH) plays an important role during the early diagenetic processes, such as for dissolution or cementation (Beaufort et al., 2007; Porter, 2010; Cuif et al., 2011; Janiszewska et al., 2017). 5) Porosity and nature of surrounding rock/sediment control the fluid migration and subsequently the amount of diagenetic alteration (Bathurst, 1975). For instance, aragonite skeletons are better preserved in conditions in which they have been rapidly sealed off from the surrounding environment by impregnable bitumines, organic films, chalk, etc. (Bathurst, 1975; Janiszewska et al., 2017). In contrast, high-Mg calcite skeletons are better preserved in clay minerals, where the porosity has been filled early by ferroan calcite (see Dickson, 2002; Stolarski et al., 2009; Gorzelak et al., 2016). 6) Physico-chemical characteristics of the diagenetic environment (i.e., meteoric, beach-rock, marine-vadose, shallow-marine, deep-marine, mixing) can promote or demote the preservation of biomineral skeletons (see Flügel, 2004). fragmentation, and bioerosion (Martin, 1999). The diagenetic history of fossil biominerals is independent of their geological age, but it is highly dependent on several other factors: 1) The original mineralogy of biominerals, including metastable or precursor phases involved in the skeletogenesis, plays an important role in the preservation potential due to mineral solubility in aqueous media (e.g., Flessa and Brown, 1983; Knoll, 2003; Cherns et al., 2011). 2) The microstructure, including polycrystalline and monocrystalline nature, crystal size, morphology, porosity of the skeleton or of its units (i.e., stereom of echinoderms) and the surface area to volume ratios of crystalline units, which modifies the specific surface area of chemical reactions (Bathurst, 1975; Flessa and Brown, 1983; Harper, 2000; Cherns et al., 2011; Gorzelak et al., 2016). 3) The total amount of the organic matrix originally present in biominerals (Hare and Abelson, 1964), and the proportion and distribution of the intra- and inter-crystalline phases. The organic matrix content can affect the solubility of material in several ways: (a) retardation of the fluid solution through a given microstructure; (b) microbial decay of organics, which releases acids favoring dissolution and precipitation of secondary minerals; and (c) organic 107 Earth-Science Reviews 179 (2018) 95–122 A. Pérez-Huerta et al. effects of diagenesis has been mainly conducted in calcium carbonate structures. They are the most abundant biominerals in the fossil record and the best-suited to record the original biogeochemistry, particularly in the case of low-Mg calcite (see Pérez-Huerta and Andrus, 2010). The biogeochemical composition of fossils is often evaluated by using cathodoluminescence microscopy (CL) and minor/trace elemental and isotopic composition of the mineral and remnant organic phases. 5.1.1. Cathodoluminescence microscopy (CL) Cathodoluminescence microscopy (CL) is an indirect, geochemical technique for detecting diagenesis, mainly used on carbonates (Barbin, 2000, 2013). During the recrystallization processes, Mn2+ and/or Fe2+ may substitute Ca2+ in the CaCO3 structure, activating a luminescence signal (e.g., Rosales et al., 2004; Frankowiak et al., 2013; Gorzelak et al., 2016). The use of this technique is based on the premise that the original calcium carbonate biominerals precipitated in equilibrium with seawater are non-luminescent under CL; therefore, non-luminescent fossil biogenic carbonates could be considered as primary structures (e.g., Czerniakowski et al., 1984; Popp et al.1986; Sælen, 1989; Grossman et al., 1996; Garbelli et al., 2012) (Fig. 15). Superficial recrystallization processes may only affect external areas of fossil skeletons in contact with the sediment and surrounding fluids producing a characteristic ring-shaped pattern as described in belemnites (Rosales et al., 2004; Benito and Reolid, 2012), brachiopods (Alberti et al., 2012), and Paleozoic corals (Coronado et al., 2013, 2015b). In addition, recrystallization (neomorphism sensu Bathurst, 1975) of non-luminescence aragonite to calcite is easily detectable under CL (due to the orange luminescence of calcite). This approach has been used for the identification of aragonite relics and several calcite cement phases (for example in Triassic scleractinian corals; see Frankowiak et al., 2013). The absence of luminescence under CL, even if the microstructure is well preserved, is not indicative of the absence of diagenetic alteration. The distinction between primary precipitated carbonate and that resulting from secondary, diagenetic precipitation is still very challenging (see Barbin, 2013). Several studies in Recent organisms with CaCO3 biominerals have shown that these pristine structures exhibit luminescent under CL (Barbin, 2000, 2013; Richter et al., 2003). Furthermore, secondary mineralization can contribute to microstructural mimicking without an associated CL signature (see Coronado et al., 2015b). 5.1.2. Minor/trace elemental and isotopic compositions of the mineral phase Conventional geochemical approaches for identifying diagenesis are often based on stable (δ13C and δ18O) and clumped isotopes, strontium and magnesium isotopes, and minor, trace, rare earth (REE) elements (see Immenhauser et al., 2016). These geochemical proxies have been used extensively in carbonate fossil biominerals, based on the assumption that such biominerals precipitated in equilibrium with the surrounding environment (see Pérez-Huerta and Andrus, 2010; Immenhauser et al., 2016). Thus, homogenous values are expected in pristine skeletons, and are easily correlated with the values of similar fossils from other geographical locations, similar diagenetic backgrounds, and with the same age (Batt et al., 2007; Armendáriz et al., 2008). The analysis of minor and trace elements (e.g., Sr, Mg, Na, Mn, Fe and S and the ratios Mg/Ca, Sr/Ca) is a common procedure to establish the primary nature of fossil carbonate biominerals. The presence of certain quantities of Mn2+ and Fe2+ are indicative of diagenesis by burial and/or meteoric waters (e.g., Popp et al., 1986). The depletion of strontium and magnesium in aragonite and calcite, respectively to values found in Recent carbonate skeletons, can aid in identifying recrystallization processes (Dauphin et al., 2007; Stolarski et al., 2009; Balthasar et al., 2011; Frankowiak et al., 2013; Coronado et al., 2015c; Gorzelak et al., 2016). Although the assumption that biominerals have precipitated in equilibrium with the surrounding environment is commonly applied, vital effects (sensu Urey et al., 1951; see also Weiner Fig. 16. EBSD mapping of ostrich (A) and dinosaur (B) eggshells showing a similar crystallographic pattern at the transition between the mammillary cone and palisade layers [Note: the sample of the ostrich eggshell was provided by Yannicke Dauphin and is part on an ongoing research collaboration. More details about the dinosaur eggshell characterization can be found in Eagle et al., 2015]. Three main “mineralogical groups” of biominerals (based on silica, phosphate and carbonate ions) may have different responses to diagenesis (including all the processes mentioned above) in many different environments. This provides multiple scenarios of biomineral alteration by diagenesis, but also can lead to unexpected, exceptional preservation. Consequently, geologists have applied numerous techniques and criteria to define the nature (primary or diagenetic) of fossil biominerals. Within this context, we take into account the most traditional approach based on the biogeochemical composition of fossils. Also, we discuss the importance of analyzing crystallographic patterns and the nanostructure of fossils to detect the effects of diagenesis. These two approaches are related to the latest advances in biomineralization and the development of high-resolution microscopy techniques. 5.1. Biogeochemical composition The use of the biogeochemical composition of fossils to detect the 108 Earth-Science Reviews 179 (2018) 95–122 A. Pérez-Huerta et al. Fig. 17. Crystallographic comparison by EBSD of basic structures in the belemnite Neohibolites minimus and Argonauta argo. MUD values refer to multiples of uniform random distribution (MUD) in relation to the orientation density distribution function, which is used to compared similarities in preferred crystallographic orientations [figure modified and adapted from Fig. 8 in Stevens et al., 2017]. nature of these fossil skeletons. More recently, sulfur chemistry of carbonates has been used to identify organic remains in fossils and whether these fossils are affected by diagenetic alteration (see Gorzelak et al., 2016). Sulfur can be present in carbonate biominerals in two ways: 1) substituting carbonate ions (Fernández-Díaz et al., 2010; Yoshimura et al., 2013) as sulfate (SO42−), and 2) in the organic matrix, probably as O-sulfate group of sulfate-polysaccharides (Dauphin et al., 2003; Cuif et al., 2008). Primary biomineral structures have higher sulfur contents than abiogenic mineral precipitates in well-preserved fossils. The sulfur content is even higher in specific skeletal regions with a specialized biological role (e.g., RADs in corals; Cuif, 2010; Frankowiak et al., 2013; Janiszewska et al., 2015; Coronado et al., 2016). and Dove, 2003) are present not just in Recent carbonate skeletons for calibration but also in fossils (e.g., Popp et al., 1986; Grossman et al., 1996; Pérez-Huerta and Andrus, 2010; Frankowiak et al., 2013; Gothmann et al., 2015). The presence of such vital effects and the unknown chemistry of past geological environments, in addition to the precise diagenetic history of analyzed fossil material, casts doubt on using geochemistry as the only valid criterion for detecting primary, pristine fossil mineralized structures. 5.1.3. Chemical composition of the remnant organic phase The evidence of a primary origin of biominerals could be acquired from the characterization of remnant organic phases in fossils. An example of this approach is the isotopic analysis (δ15N, δ34S, δ13C and δ18O) of isolated organic matrices from fossil coral and bivalves (Cuif et al., 2011; Dreier et al., 2014; Frankowiak et al., 2016; Tornabene et al., 2017). The finding of similar isotopic composition of these organics with those present in extant taxa has supported the primary 5.2. Analysis of crystallographic patterns Biological control of crystallographic properties is a distinctive 109 Earth-Science Reviews 179 (2018) 95–122 A. Pérez-Huerta et al. (caption on next page) 110 Earth-Science Reviews 179 (2018) 95–122 A. Pérez-Huerta et al. Fig. 18. Biomineral characteristics of the fossil rugose coral Bothrophyllum. A. Transmitted light microscopy image that shows a transversal cut of Bothrophyllum sp. skeleton from Covadonga section (Las Llacerias Formation, Asturias, Spain, of Kasimovian age, Upper Carboniferous). Black-squares indicate the areas of EBSD and polarized microscopy image in C). B. Image showing the minor and major septa of coral. Note that black squares indicate the location of EBSD maps. C. Polarized microscopy image showing the fibro-normal microstructure of Bothrophyllum in a contact area (whiter arrow) between a major septum and a minor septum (RAD: Rapid Accretion Deposits; TD: Thickening Deposits; mS: minor septum). D–E. Detailed crystallography by EBSD of a major septum, showing the RAD and TD areas analyzed (1 refers to pole figures in F image and 2 to G image): D. Index intensity map, showing the microstructure composed of small fibers. Note some evidence of dissolution (white arrow); E. Crystallographic orientation map, showing two mainly crystallographic orientations, one in the TD with a high crystallographic control and other in RAD with a low crystallographic control. F–G, J. Pole figures in normal direction view (ND) to the sample surface in a three axes reference system with indication of the reference (X0) and transverse (Y0) directions: F. Pole figures of region 1 (TD), indicating crystallographic orientation of calcite crystals in reference to the {001}, {010} and {104} planes; and crystallographic key indicating color coding of crystallographic axes; G. Pole figures of region 2 (RAD), indicating the random crystallographic orientation of calcite crystal in reference to the {001} and {010} planes. Note the misorientation image of the fibers highlighted in the image (H), where can be observed that they are formed by small crystallographic domains. H–I. Index intensity map and crystallographic orientation map of a detail of the TD area. Note that the fibers are forming boundless of small fibers with a well-controlled orientation (J). J. Pole figures of a TD region, indicating crystallographic orientation of calcite crystals in reference to the {001}, {010} and {104} planes. Fig. 19. Nanostructural characterization of secondary calcitic cement. AFM images of an inorganic calcite showing that is not formed by distinctive nanogranules and dark envelopes as biogenic calcite (A, D - height images; B, E - phase images and C, F - amplitude images). Small acicular nanocrystals are presented at high magnification, very well organized forming clear and flat steps of growth. comparing with those present in abiogenic minerals. For example, Stolarski et al. (2007) showed differences in the lattice parameters and anisotropic distortions of the biogenic lattice of a Cretaceous calcitic scleractinian coral in comparison with synthetic calcite. Another path is to compare crystallographic patterns in fossils to modern representatives (see Cuif et al., 2011, 2012). In case of extinct taxa, the best approach is to make a comparison with phylogenetically close organisms, as shown for the case of dinosaur eggshells (Fig. 16; e.g., Eagle et al., 2015; Moreno-Azanza et al., 2017). An alternative is to compare the crystallographic features of fossils to those present in Recent organisms that are believed to have similar mechanisms for biomineralization. This is perfectly illustrated in a recent analysis of the biomineralization in belemnites (Fig. 17; see Stevens et al., 2017). The last approach is to analyze the biological meaning of preferred crystallographic orientations in the context of the assembly of a complete structure (i.e., coral skeleton; see Coronado et al., 2015a, 2016) and its functional morphology. For example, we present here a case of good preservation in the rugose coral Bothrophyllum to illustrate this point (Fig. 18). In the analysis of a major septum with fibro-normal microstructure (Fig. 18B–C), fibers are oriented perpendicular along the septa. In the region of Thickening Deposits (TD), the c-axis of calcite is parallel to morphological axis of crystals (Fig. 18B–D, H), whereas aand b-axes are rotating around the c-axis forming a turbostratic distribution (Fig. 18F), as can be appreciated in the crystallographic plane feature of biominerals (see Section 2), and to the extent that it can be applied in phylogenetic studies (Raup, 1962). Recent results in the analysis of lattice properties of biominerals have underlined that they have distinctive, anisotropic lattice distortions related to organic contents and chemical impurities (i.e., magnesium) (see Zolotoyabko, 2017). Thus, the study of crystallographic patterns (i.e., preferred crystallographic orientations and degree of crystallization) of fossil biominerals can be very robust approach in identifying the primary nature of fossil skeletons. Polycrystalline skeletons formed from microstructures are characterized by preferred crystallographic orientations and unique arrangements in specialized structures, such as the septa of scleractinian corals (Mouchi et al., 2017). These crystallographic patterns can be compromised by diagenetic alteration, replacing the original, biological control for a random orientation regulated by abiogenic (geological) processes. For example, this has been observed in fossil molluscs using polarized microscopy, presenting random polarization of carbonate crystals after diagenesis (e.g., Sandberg and Hudson, 1983; Maliva and Dickson, 1992). Recent approaches using newly developed techniques (i.e., EBSD and CIP) have been focused more on finding original crystallographic patterns of primary structures rather than diagenetic ones (e.g., Pérez-Huerta et al., 2007a, b; Coronado et al., 2013, 2015a; Torney et al., 2014; Stevens et al., 2017). Biological crystallographic attributes can be found in biominerals by 111 Earth-Science Reviews 179 (2018) 95–122 A. Pérez-Huerta et al. Fig. 20. Trilobite eye. A. SEM image of a Phacops schizocroal eye showing the arrangement of the calcite lenses. B. EBSD characterization of a lens: Left (top) - crystallographic map of a single lens in cross section, with colors representing different calcite crystallographic planes, adjacent to the sclera and limestone; Left (bottom) - Orientation tolerance map of the lens above, showing that all of the lens calcite is within 30° of the reference point (R) (scale bar = 200 μm); Right (top) - pole figure showing the orientation of calcite in the center of the lens shown in left (top); c denotes the c-axis, a denotes the a-axis, m denotes the pole to {10–10}, and the unlabelled points are the poles to {4–130} planes; Right (bottom) - pole figure of the whole lens shown in left (bottom), with the same color coding. The pole figure shows that most of the changes in crystallographic orientation within the radial fringe can be described by rotation about the a-axis (i.e. the center of the pole figure) and the rotation is asymmetric [figures modified and adapted from Figs. 2 and 7 in Torney et al., 2014]. from the median septa (Fig. 18C–E). These crystals are randomly distributed in all the crystallographic planes, regardless of their morphological axes, indicating that they are secondary after recrystallization. This process of recrystallization is common in fossil aragonitic and {104}. This distribution has been described previously in other Paleozoic corals (Coronado et al., 2015b; Coronado et al., 2016) and Recent molluscs (Checa et al., 2007a). In contrast, the crystals of Rapid Accretion Deposits (RAD) are short fibers oriented forming a fan shape 112 Earth-Science Reviews 179 (2018) 95–122 A. Pérez-Huerta et al. (Coronado et al., 2015c). However, a survey of a large number of spicules from the same locality indicates that such preferred crystallographic orientation is not preserved in all of them (Coronado et al., 2015c). 5.3. Analysis of nanostructures Beginning with the assumption that biominerals are characterized by a unique nanostructure (see Section 2), well-preserved fossil microcrystals should display such characteristic nanostructures. The combined use of FEG-SEM and AFM has allowed observation of nanostructures with many shapes (i.e., granules, rods, bars, sticks, pills, etc.) and sizes in fossilized microstructures (Fig. 13; see Cuif et al., 2011; Coronado et al., 2013, 2016). It is characteristic that these nanocrystals, in most of cases, are aggregated in co-oriented textures inside the microcrystals (Fig. 13E–G, K; Dauphin, 2002; Cuif et al., 2011; Coronado and Rodríguez, 2016; Coronado et al., 2016), forming submicrolaminae (Fig. 13C, F, I; see also Coronado and Rodríguez, 2016), fibers (Dauphin, 2002; Cuif et al., 2011; Coronado et al., 2015c), and mineral bridges (sensu Checa et al., 2011) (Fig. 13I). The nanocrystals exhibit dark envelopes surrounding them, which occasionally are 5–10 nm thick and have a clear relief in amplitude mode under AFM (Fig. 13H). These dark coatings are interpreted in Recent organisms as a mix of amorphous and organic phases involved in crystallization (Cuif et al., 2011; Pérez-Huerta et al., 2013a, b). The presence of diagenetic recrystallization results in a total or partial obliteration of these nanostructures, even if recrystallization processes have replicated the microstructure. This can be observed during silicification of carbonate skeletons, in which secondary silica does not have any nanotexture; meanwhile, the original biomineral structures retain a characteristic granular nanostructure (Fig. 15). In the case of recrystallization by the same mineral phase (i.e., biogenic calcite replaced by diagenetic calcite), even in cases of epitaxial growth, the secondary, diagenetic phase (i.e., cement) is featureless at the nanoscale (Fig. 19; see also Stolarski et al., 2009; Coronado et al., 2015c; Gorzelak et al., 2016). These findings suggest that the best way to detect the effects of diagenesis and the presence of primary biominerals is by looking at nanostructures in fossils. However, the use of FEG-SEM and AFM for this purpose is time-consuming and challenging and thus, does not provide a quick assessment of fossil preservation. In contrast, the observation of crystallographic patterns is easier and equally useful and, possibly, a more rapid approach for the evaluation of diagenesis. 6. Potential research areas The application of current biomineralization knowledge to the fossil record opens new possibilities for paleontological research. Below, we provide three examples related to: 1) new biomaterials inspired by fossils; 2) molecular paleontology; and 3) interpretation of geological events aided by the analysis of fossil biominerals. Fig. 21. Crystalline lenses in brittlestar and chiton. A. SEM image of the arrangement of calcite lenses (dashed red lines) on an arm plate [image taken by Raya Greenberger]; B. SEM images and optical model for the same lenses as in A [figure modified and adapted from Fig. 1 in Aizenberg et al., 2001]. C. Optical image of the arrangement of aragonite lenses (red arrows) on the exoskeleton of a chiton [image taken by Raya Greenberger]. D. Optical model for the vision in the same chiton lenses as in C [figure modified from Fig. 4 in Speiser et al., 2011]. 6.1. Fossil biominerals and biomaterials Throughout the course of evolution, mineralizing organisms have acquired the ability to produce multifunctional and complex hierarchical structures with excellent mechanical properties that cannot be duplicated with synthetic materials and modern technologies (Meyers et al., 2006). Within this context, materials scientists have primarily focused their attention on the complex nature of biominerals because of their excellent mechanical properties (e.g., Lin et al., 2006; Meyers et al., 2008; and see references in Yang et al., 2011). Among biominerals, a common target of interest has been those composite structures based on calcium carbonate (CaCO3) minerals (i.e., nacre) that have a primary protective function, and in some cases with additional dual or multi-functionality purposes (e.g., Romano et al., 2007; Li and Ortiz, 2013). calcitic scleractinians (Stolarski, 2003; Stolarski et al., 2007; Frankowiak et al., 2013). These approaches in the analysis of crystallographic patterns in fossil are useful but caution should be exercised in the case of secondary recrystallization mimicking the original microstructure (e.g., PérezHuerta et al., 2007a, b; Coronado and Rodríguez, 2016). For example, this can be shown for the recrystallization of Alcyonaria spicules retaining the original c-axis orientation of the carbonate mineral phase 113 Earth-Science Reviews 179 (2018) 95–122 A. Pérez-Huerta et al. Fig. 22. Comparison of the biomechanics for articulation of chiton (A; figure adapted from Fig. 1 in Connors et al., 2012) and trilobite, with arrow indicating the location of the pygidium beneath the cephalon (B – scale bars = 5 mm; figure adapted from Fig. 9 in Yuan et al., 2014) skeletons. 114 Earth-Science Reviews 179 (2018) 95–122 A. Pérez-Huerta et al. Fig. 23. Comparison of organic characterization extracted from biominerals prior and after the latest development on genomics/proteomics. A. Polyacrylamide gels of the organic fraction extracted from the Cretaceous fossil Scabrotrigonia thoracica; the arrow indicate the presence of bands of high molecular weight in fossil shells [figure adapted from Fig. 2 in Weiner et al., 1976]. B. Comparison of prism and nacre SMPs of Pinctada margaritifera and Pinctada maxima; prisms and nacre proteins identified in both bivalve species by MS/MS analyses are circled in blue/green or red/orange, respectively, and numbers represent common proteins to both structural layers and in between species [figure adapted from Fig. 2 in Marie et al., 2012]. trilobite eyes, with calcite lenses, remarkably advanced our knowledge of the evolution of visual systems and the understanding of the ecological success of this group of arthropods (Fig. 20; Clarkson and LeviSetti, 1975; Clarkson, 1979). Also, recent data on trilobite eyes, gained by applying newly developed techniques, has expanded the analysis of biomineralization in visual systems (e.g., Lee et al., 2007, 2012; Torney The study of “living fossils” has been also applied to biomaterials research (e.g., Bruet et al., 2008). However, the analysis of the fossil record can be deeper beyond that of the “living fossils” concept. The study of fossils can even anticipate finding remarkable biomaterials before their description in extant taxa. This is the case of crystalline lenses evolved for photoreception and 3D vision. The description of 115 Earth-Science Reviews 179 (2018) 95–122 A. Pérez-Huerta et al. Fig. 24. Example of organics found in dinosaur bones. Top. Fragments of blood vessels from Tyrannosaurus rex bones [figure modified and adapted from Fig. 3 in Schweitzer et al., 2005]. Bottom. Fiber fragments identified as bone collagen fibrils; the arrow indicates fibers analyzed to determine the banding periodicity in a comparison to a generic collagen molecule [scale bars = 200 nm (left) and 100 nm (right); figure modified and adapted from Bertazzo et al., 2015]. diagenesis (e.g., Towe, 1980; Logan et al., 1991). Within the context of understanding biomineralization, the analysis of preserved organic components in fossil mollusc shells was remarkable, and a pioneering work for the further development of this study in extant taxa (Fig. 23A; Weiner et al., 1976). Due to reasonable doubt in the reliability of the information provided by fossil organics (e.g., Sykes et al., 1995), the field of molecular paleontology for biomineralization research declined after 1990s. However, there are two main arguments that would justify the “rebirth” of molecular paleontology to better understand the evolution of biomineralization and adaptation of metazoans throughout the Phanerozoic. Firstly, new advances in genomics and proteomics have contributed to improve our knowledge of the molecular toolkit involved in the biomineralization of extant organisms (Fig. 23B; e.g., Marin et al., 1996, 2014; Marie et al., 2012; Drake et al., 2013). Also, innovative protein sequencing protocols have enabled a proper comparison of organics in fossil organism to their Recent counterparts (e.g., Demarchi et al., 2016). The second argument relates to newly developed techniques for the characterization (microscopy and spectroscopy) and extraction of organics in fossil from the deep Phanerozoic record. For example, preserved tissues (i.e., vessels) and organic components (i.e., collagen) have been reported in dinosaur bones (Fig. 24; Schweitzer et al., 2005, 2013; Bertazzo et al., 2015). Although not exempt from controversy (see Demarchi et al., 2016), such discoveries in these fossil bones open a new venue of exploration for biomineralization in the fossil record. et al., 2014). Besides the paleontological insight, the analysis of these trilobite lenses contributed to the understanding of calcite lenses that are optimized for photoreception as found in modern brittlestars (Fig. 21A; Aizenberg et al., 2001). Subsequently, the more recent analysis of mineral lenses in some chiton species (Fig. 21B–C; Speiser et al., 2011) has contributed to the debate over the advantages of having calcite vs. aragonite as the base polymorph for lens composition. On the other hand, the application of modern approaches to biomineralization research can undoubtedly increase our understanding of the importance of fossil biominerals for functional morphology and ecological adaptation. For example, the biomechanics of chiton skeletons (Fig. 22A; Connors et al., 2012) can contribute to a better understanding of the articulation of trilobite exoskeletons (Fig. 22B; e.g., Yuan et al., 2014). In summary, because organisms have the ability to generate, with ease, amazingly complex and functional inorganic structures (Kröger, 2009), any source of bio-inspiration for new biomaterials and biomimicry should be exploited. The fossil record, with its vast diversity of preserved biominerals, is then a logical, largely unexplored choice. 6.2. Molecular paleontology The fundamental interplay of organic components with crystalline mineral phases is responsible for the functionality and diversity found among biomineral structures (e.g., Lowenstam and Weiner, 1989; Mann, 2001; Cuif et al., 2011). The study of the organic matrix is then essential to understanding biomineralization processes (Marin et al., 2014), and this can be aided by the study of fossil organisms. Abelson (1954) recognized the potential preservation of the organic matrix in fossils. Subsequently, discoveries related to exceptional preservation (e.g., Towe and Urbanek, 1972) reinforced the idea that organics from fossils could be analyzed. Arguably, these were the pillars for the development of molecular paleontology, and it has had an important place in paleontological research for about four decades (1960s–1990s). The study of organics in fossils was directed to mainly understand phylogenetic relationships (e.g., Jope, 1967; Mitterer, 1978) and the preservation potential of fossils and the effects of 6.3. Geological events and biomineralization Traditionally, the understanding of biomineralization and the fossil record has been linked primarily to the phylogeny of metazoans (e.g., Knoll, 2003), evolutionary trends through Earth's history (e.g., Kidwell, 2005), the Cambrian Explosion and the emergence of widespread biological mineralization (Knoll and Carroll, 1999; Porter, 2010; e.g., Wood and Zhuravlev, 2012), exceptional fossil preservation (e.g., Towe and Urbanek, 1972; Stankiewicz et al., 1997; Schweitzer et al., 2005; 116 Earth-Science Reviews 179 (2018) 95–122 A. Pérez-Huerta et al. Fig. 25. Biomineralization and Aragonite-Calcite Seas. Top. Aragonite-Calcite sea variation throughout the Phanerozoic with a comparison of the mineralization in corals [figure adapted from Fig. 1 in Janiszewska et al., 2017]. Bottom (left). Illustration of the Late Cretaceous calcitic coral Coelosmilia sp. [figure adapted from Fig. 1 in Stolarski et al., 2007]. Bottom (right). SEM images of relic aragonite (relics circled in B) in Ordovician-Silurian brachiopods [scale bars in A = 20 μm and B = 50 μm; figure adapted from Fig. 2 in Balthasar et al., 2011]. in biomineralization research. Exceptions to this trend (e.g., Cuif et al., 2011 and references therein; Lee et al., 2012; Coronado et al., 2013; Torney et al., 2014; Coronado et al., 2015a, c; Stevens et al., 2017) have resulted in major advances in recognizing primary biogenic structures in fossils, the clarification of phylogenetic questions, choosing better Nance et al., 2015), and the use of biomineralized structures for paleoclimatic and paleoenvironmental reconstructions (e.g., Urey et al., 1951; Immenhauser et al., 2016). Most of these connections have been established from a geological perspective and, mainly, without incorporating a biological point-of-view and the most recent knowledge 117 Earth-Science Reviews 179 (2018) 95–122 A. Pérez-Huerta et al. Fig. 26. Biomineralizaton and ocean acidification (OA). A. Calcite and aragonite growth in a mussel under different OA scenarios [figure modified and adapted from Fig. 4 in Fitzer et al., 2016]. B. Geochemical changes related to OA across the Permo-Triassic mass extinction interval (black arrow) [figure modified and adapted from Fig. 2 in Clarkson et al., 2015]. calcite and vice versa in response to seawater chemistry changes (e.g., Checa et al., 2007b). Otherwise, without the correct molecular control, an organism will produce only one polymorph independently of environmental changes. Finally, the discovery of fossil exceptions to the “Aragonite-Calcite Seas” idea is increasing rapidly (Fig. 25; Stanley et al., 2002; Stolarski et al., 2007, 2016; Balthasar et al., 2011; Janiszewska et al., 2017). Such exceptions are already quite numerous becoming rather the norm in the fossil record. Another example of using current biomineralization research to decipher the impact/record of geological events in the fossil record is related to climatic and environmental changes. Recent studies have shown that rapid warming events and ocean acidification changes impact the biomineralization of marine calcifiers (Fig. 26; e.g., PérezHuerta et al., 2013b; Fitzer et al., 2016). In parallel, significant geological events (i.e., mass extinctions) have been related to warming and more recently to ocean acidification (Permo-Triassic Mass Extinction; Fig. 26; Clarkson et al., 2015). Therefore, these hypotheses could be tested by further analyzing calcium carbonate biominerals in fossil invertebrates. material for geochemical analyses, and the understanding of functional morphology of fossil biominerals. We argue that applying the most recent knowledge of biomineralization can contribute to our understanding of geological events and trends throughout the Phanerozoic. This can be the case for a prevailing hypothesis in geosciences linking the composition of calcifying marine organisms and the carbonate chemistry of the ocean (Balthasar et al., 2011 and references therein). The “Aragonite-Calcite Sea” concept has been used to explain the evolution of calcareous biomineralization (Fig. 25; e.g., Hardie, 1996; Stanley and Hardie, 1998; Ries, 2005; Porter, 2010; and see Balthasar and Cusack, 2015 for further references). This concept is based on the idea that the Phanerozoic sea molar ratio of Mg:Ca is the main influence on the calcium carbonate polymorph secreted by organisms during mineralization (Hardie, 1996; Stanley and Hardie, 1998; see also Balthasar and Cusack, 2015). However, this concept contradicts our current understanding of biologically-controlled mineralization by eukaryotes involving the use of ACC, and its interplay with Mg2+ and organics, in CaCO3 biomineralization (see Wang et al., 2009 and references therein). Furthermore, it diminishes the genetic/molecular control in regulating biomineralization. Recent studies of biomineralization genomics/proteomics indicate that there are specific “molecular toolkits” that are involved in controlling polymorph type, especially in CaCO3 (see Marie et al., 2012; Marin et al., 2014). This implies that a given organism must have the “molecular toolkit” that allows switching from secreting aragonite to 7. Concluding remarks Throughout this contribution, we have emphasized the study of biomineralization for a better understanding of the fossil record. The analysis of fossils (i.e., trilobite lenses) has proven to contribute to 118 Earth-Science Reviews 179 (2018) 95–122 A. Pérez-Huerta et al. biomineralization research in extant taxa as well. Recognizing primary, biogenic structures in fossils and the effects of diagenesis is important in the use of fossils in geochemistry, in the understanding of metazoan evolution, and in the correct interpretation of how geological events impacted the biosphere. Also, the analysis of preserved organics in fossils helps us understand fossil preservation and the making up of the fossil record. All this knowledge is underpinned by the latest research in the field of biomineralization and the rapid development of characterization techniques for Recent and fossil biominerals. Overall, this review is a starting point for discussing the importance of biomineralization in paleontological research and even, in a broader sense, in geosciences. 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Clarkson, M.O., et al., 2015. Ocean acidification and the Permo-Triassic mass extinction. Science 348, 229–232. Cody, G.D., et al., 2011. Molecular signature of chitin-protein complex in Paleozoic arthropods. Geology 39, 255–258. Connors, M.J., et al., 2012. Three-dimensional structure of the shell plate assembly of the Acknowledgements Alberto Pérez-Huerta greatly thanks Dr. Fernando Alvarez (Universidad de Oviedo) for sharing the beauty and significance of paleontology many years ago, and the continuous support and friendship. APH appreciates the ongoing support, advice, and teachings about biomineralization by Dr. Maggie Cusack, Dr. Jean Pierre Cuif, Dr. Yannicke Dauphin, Dr. Lia Addadi, and Dr. Steve Weiner. In addition, APH acknowledges the significant, current contribution of the following geologists to the field of biomineralization: Dr. Nita Sahai (University of Akron), Dr. Patricia Dove (Virginia Tech), Dr. Rinat I. Gabitov (Mississippi State University), Dr. Maggie Cusack (University of Stirling), Dr. Juan Diego Rodríguez-Blanco (Trinity College Dublin), Dr. Nicola Allison (University of St. Andrews), Dr. Antonio G. Checa (Universidad de Granada), Dr. Alejandro Rodríguez-Navarro (Universidad de Granada), Dr. Jean Pierre Cuif (Muséum National d'Histoire Naturelle, Paris), Dr. Yannicke Dauphin (Muséum National d'Histoire Naturelle, Paris), Dr. Frederic Marin (Université de Bourgogne), Dr. Claire Rollion-Bard (Institut de Physique du Globe de Paris), Dr. Wolfgang Schmahl (LMU München), Dr. Erika Griesshaber (LMU München), Dr. Jarosław Stolarski (Polish Academy of Sciences), Dr. Anders Meibom (Ecole Polytechnique Federale de Lausanne), Dr. Kazuyoshi Endo (The University of Tokyo), and Dr. Dorrit E. Jacob (Macquarie University). Also, APH acknowledges financial support from the US National Science Foundation (EAR-1226832, 1402912 and 150779 grants), the Office of the VP for Research and Economic Development, the College of Arts & Sciences, and the Department of Geological Sciences of the University of Alabama. Ismael Coronado acknowledges support by the National Science Centre, Poland research grant 2015/19/B/ST10/02148 and by the Spanish Ministerio de Economía y Competitividad (research project CGL2016-78738-P) and Complutense University Research Group (910231). Finally, authors thank the editor, Dr. André Strasser, and two anonymous reviewers for their help in improving the quality of the present contribution. References Abelson, P.H., 1954. Organic constituents of fossils. In: Carn. Inst. Wash. Yearb. 53. pp. 97–101. Addadi, L., Raz, S., Weiner, S., 2003. Taking advantage of disorder: amorphous calcium carbonate and its roles in biomineralization. Adv. Mater. 15, 959–970. 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