Abstract

Fossil skeletal apatites vary in their composition and can yield mixed biochemical, environmental and diagenetic information. Thus, it is important to evaluate the diagenesis spatially inside the skeleton. We study the cross sections of shells of the Furongian lingulate brachiopod Ungula ingrica from Estonia using the Attenuated Total Reflectance – Fourier Transform Infrared (ATR-FTIR) microspectroscopic and energy dispersive spectroscopic (EDS) mapping and show for the first time that different structural laminae of the shell have different chemical compositions. Compact laminae are rich in PO43−, Na, Mg and poor in F and Ca. Porous (baculate) laminae are rich in carbonate anions, Ca and F, but contain less Na and Mg. The ATR-FTIR spectra show further differences in the ν2 carbonate region, where the IR band at 872 cm−1 in compact laminae is replaced by a strong band at 864 cm−1 in baculate laminae. The changes in shell apatite suggest different origins of the apatite phases. Compact laminae are likely chemically less altered and could potentially carry more reliable palaeoenvironmental or geochemical information than the apatite in baculate laminae, which is mostly authigenic in its origin.

Keywords

  1. Apatite
  2. attenuated total reflectance mapping
  3. Cambrian
  4. diagenesis
  5. Estonia
  6. lingulate brachiopod
Brachiopods are benthic marine animals that mostly secrete their valves of low-Mg calcite (e.g. Brand et al. ) or Ca-phosphate apatite (linguliform brachiopods; Cusack & Williams ). The geochemical composition of fossil calcitic brachiopods is widely used to characterize ancient marine environmental conditions (e.g. Veizer et al. ; Brand ; Came et al. ; Giles ). Calcitic valves of brachiopods are commonly secreted in equilibrium with sea water (Brand et al., ; Parkinson et al. ) and consequently record the properties of the seawater at the time of animal life, while low-Mg calcite is not easily recrystallized during diagenesis (e.g. Al-Aasm & Veizer ). The use of linguliform brachiopods or any other bioapatitic fossil as palaeoenvironmental proxies is, however, largely hampered by vital effects on phosphate secretion and significant diagenetic alteration of bioapatite (e.g. Lécuyer et al., ; Wenzel et al. ; Rodland et al. ; Bassett et al. ; Tütken et al. ). Therefore, a full range of diagenetic changes should be considered to assess the usefulness and reliability of palaeoenvironmental or ecological information possibly recovered form biomineralized apatitic tissues (Trueman ).
Shells of linguliform brachiopods are deposited as mineralized laminae alternating with organic-rich laminae (Cusack et al. ; Williams & Cusack, ). The organo-phosphatic laminated shells of different linguliform brachiopod genera are of various microstructural complexity (Williams et al., ; Cusack et al. ; Williams & Cusack ; Streng et al. ). Baculate shell structure, characterized by alternating compact and baculate laminae, is typical of Palaeozoic linguloid brachiopods (Cusack et al. ). Compact laminae are composed of tightly packed apatite crystals. Baculate laminae are formed of trellized apatitic rods (bacula), which are supposed to have been enmeshed into organic matrix at the lifetime of the brachiopod as in modern brachiopods (Williams & Cusack ).
Earlier studies have shown that despite the poor fossilization potential of living lingulates (e.g. genera Glottidia Dall ; Lingula Bruguière ) (Emig ; Kowalewski ), the structure and mineral parts of fossil lingulate shells can be preserved in extraordinary detail. Comparing Carboniferous and modern Lingula, Cusack & Williams demonstrated that the structure and mineral parts of a shell may be preserved in nanometric detail. Lang et al. and Lang & Puura described the originally organic but apatite-replaced nanofibrils, representing the finest parts of the hierarchical construction of the shells of Cambrian lingulates Obolus ruchini Khazanovitch & Popov (in Khazanovitch et al. ) and Ungula inornata (Mickwitz ). However, the preservation at ultrastructural level is not common and may vary even within a single shell (Lang et al. ).
Because of microstructural differences in alternating more compact laminae and more porous baculate laminae, the lingulate shells provide two different environments for diagenetic precipitation and recrystallization processes. Earlier mineralogical studies of shell apatite of living lingulates show a fluoride-containing carbonate-OH-apatite composition (Puura & Nemliher ). However, Lécuyer et al. suggested that at least 12 wt% of secondary apatite could have been added to the in vivo precipitated apatite during the degradation of the organics in the lingulate shells. Indeed, in fossil brachiopod shells, two apatite phases (interpreted as skeletal and non-skeletal apatite) have been detected using X-ray diffraction (XRD) analysis of bulk shell material (Puura & Nemliher ; Nemliher et al. ). These phases suggest that shell microstructures are composed of apatite that precipitated and/or recrystallized in different diagenetic conditions and possibly at different rates and times. However, it is not known where the different apatite phases are located in the shell structure and to which extent their compositions differ from each other.
The purpose of this article is to study the chemical variability of apatite in a fossil lingulate brachiopod Ungula ingrica (Eichwald ) using combined analytical scanning electron microscopy (SEM), XRD and infrared (IR) microspectroscopic study of the shells. Ungula ingrica has a baculate shell structure (Holmer ) and is one of the most common brachiopods in the Cambrian – Ordovician boundary beds in Estonia and NE Russia (Heinsalu & Viira ). The shells of U. ingrica commonly form lingulate coquinas that locally may comprise shelly phosphorite beds of economic interest (Raudsep ).
We aim to localize different apatite phases within the shell and understand apatite diagenetic replacement and/or recrystallization patterns with respect to the baculate stratiform structure of these brachiopods. The locations in brachiopod shells, that are chemically less altered than others, are indicated. These could potentially be used for acquisition of more reliable palaeoenvironmental-geochemical data from fossil lingulate brachiopods.
Attenuated Total Reflectance (ATR) mapping using Fourier Transform Infrared (FTIR) microscopy in the ATR mode is employed here for the first time to characterize the composition of fossil linguliform brachiopod shells. This method is based on the vibrations of certain bonds in molecules or ions in a phase when irritated with IR light and allows a detailed micro-scale differentiation of apatite compositional variations. Recently, it has also been adapted to study spatial diagenesis in bones (e.g. Reiche et al. ; Lebon et al. ) and to characterize the structure and composition of phosphatized and/or organic microfossils (e.g. Igisu et al. ).

Material and methods

Geological setting

Ungula ingrica valves were collected from the Furongian Kallavere Formation exposed in the Iru and Ülgase outcrops, North Estonia (Fig. ). Both sections expose light grey sandstones with occasional thin greenish-grey clay beds of the Ülgase Formation, overlain by brownish to yellowish-grey sandstones of the Kallavere Formation. The sandstones in the Kallavere Formation yield abundant lingulate brachiopods that form coquinas at several levels (Puura, ). Common brachiopods in the coquinas are Ungula ingrica, Schmidtites celatus (Volborth ) and Keyserlingia buchii (de Verneuil ). The upper part of the formation shows intercalations of organic-rich black shale beds (Puura ).
Fig. 1. Generalized map of Estonia and nearby areas, showing the location and the sections of the Iru and Ülgase outcrops (after Puura, ). The sample locations are indicated with horizontal black boxes. The shells from Iru originate from two levels – Iru5 and Iru7. 1, kerogenous shale; 2, lingulate coquina and conglomerate; 3, sand and sandstone yielding lingulate debris; 4, sand and sandstone; 5, lingulate brachiopods; 6, redeposited lingulate brachiopods; 7, conodonts and graptolites; 8, part of a range with no occurrences documented. Mbr, Member.
Based on the occurrence of conodonts Westergaardodina cf. bicuspidata and Furnishina furnishi at the base of the Kallavere Formation, the lower part of the formation is correlated with the Furongian Peltura scarabeoides trilobite Biozone (Heinsalu et al. ). The Cambrian – Ordovician boundary is drawn in these sections within the Kallavere Formation, at the first appearance of the conodont Cordylodus lindstromi a few metres above the base of the formation (Heinsalu & Viira ; Puura & Viira, ).
The sedimentological characteristics of the sections suggest deposition in a marine setting within a peritidal/beach zone of a shallow epicontinental sea (Artyushkov et al. ). During the Furongian and Cambrian – Ordovician transition, the Baltica palaeocontinent was located on the southern hemisphere at intermediate to high southerly latitudes (Torsvik et al. ).

Material and sample preparation

Altogether 14 complete valves of Ungula ingrica (ten from the Iru and four from the Ülgase outcrop, listed in Table ) were selected from the lingulate coquinas in the middle and lower parts of the Kallavere Formation. The valves from Iru originate from two levels (Iru5 and Iru7 in Fig. ). The preservation state of shells from these two levels is similar, however, the shells from the upper coquina (Iru7 in Fig. ) are more commonly pyritized. In the initial phase of study several valves from both coquinas in Iru and from the coquina in Ülgase were embedded into plastic (polymethyl methacrylate, PMMA, Varikleer) resin. The embedded samples were then ground with silicon carbide papers in successive finer steps and finally polished with diamond paste of 1 μm grain size. The polished cross sections of valves were further studied by means of FTIR microscopy in ATR mode, analytical scanning electron microscopy (SEM-EDS) and optical microscopy (OM). Two valves (sample Iru5 from Iru and one from Ülgase) were chosen for detailed mapping presented in this study. For comparison a shell of modern Lingula anatina Lamarck ; from Cebu Island, the Philippines, was studied.
Table 1. List of the studied samples
SampleCollection numberLocalityAnalyses
U. ingrica (I-I5-d)TUG 1323-5Iru5XRD
U. ingrica (I-I5-v2)TUG 1323-5Iru5XRD
U. ingrica (I-I5-v)TUG 1323-5Iru5XRD
U. ingrica (Iru7)TUG 1323-5Iru7XRD
U. ingrica (I-I7-v2)TUG 1323-5Iru7XRD
U. ingrica (I-I7-v3)TUG 1323-5Iru7XRD
U. ingrica (I-I7-v)TUG 1323-5Iru7XRD
U. ingrica (I-Ü-3-d)TUG 1323-5ÜlgaseXRD
U. ingrica (I-Ü-3-v2)TUG 1323-5ÜlgaseXRD
U. ingrica (I-Ü-3-v)TUG 1323-5ÜlgaseXRD
U. ingricaTUG 1323-6Iru5ATR-FTIR microspectroscopy, SEM-EDS, OM
U. ingricaTUG 1323-7Iru7SEM
U. ingricaTUG 1323-8ÜlgaseATR-FTIR microspectroscopy, OM
U. ingricaTUG 1323-9Iru7SEM (Pt coated)
Lingula anatina (recent)GIT 587-32Cebu Island, the PhilippinesATR-FTIR microspectroscopy
The ATR mapping measurements were performed in the ATR mode with the Thermo Scientific Nicolet iN10 MX FT-IR microscope, equipped with a MCT detector cooled by liquid nitrogen. The measurements were performed using a slide-on ATR objective with a conical germanium crystal, in the wavenumber range 4000–550 cm−1, at a spectral resolution of 4 cm−1 and the number of scans 8 was used. The ATR maps varied in size, being composed of 861–3915 spectra. The selected areas were analysed with a step size between 7 and 25 μm. The particular step size of scanning was chosen according to the characteristics of the area of interest on the sample to ensure that the nature of the thinnest observable laminae would be recorded. For the ATR-FTIR spectra in the maps no additional specific corrections (ATR-correction, baseline correction, etc.) were carried out to avoid possible distortions of the IR spectra. More detailed discussion on the effects of ATR-correction and the ATR phenomenon can be found in Vahur et al. The data were collected and processed using Thermo Electron's OMNIC PICTA software. The spectral maps acquired were further processed by means of OMNIC PICTA software into maps of intensity ratios of bands of two wavenumbers of interest. Intensity ratios rather than absolute (integral) intensities were used to make the spectra of different samples comparable, and to eliminate the signal changes originating from the variations in the ATR crystal contact. As in this process the peak heights are corrected, a more realistic result is obtained than with the maps created by using the wavenumber of one band only. This approach allows us to observe the spatial variation in relative spectral intensities across the cross section of the brachiopod shell.
Different shells were used for XRD analysis because the material is destructed during preparation. Ten single valves of Ungula ingrica (seven from Iru, three from Ülgase, Tables  and ) were analysed. Valves were hand-ground with an agate mortar and pestle, and XRD preparations were made on a zero-background silicon mono-crystal sample holders for mineral analysis. X-ray diffraction patterns were collected with a Bruker D8 Advance diffractometer with Cu radiation using a LynxEye linear detector. The mineral composition and structure refinement of apatite phases were modelled using the Topas 4 code.
Table 2. Refined lattice parameter values for two apatite phases (A1 and A2)
SampleA1 (Å)A2 (Å)
acac
I-I5-d9.3466.8969.3916.891
I-I5-v29.3446.8979.3946.894
I-I5-v9.3426.8999.3776.896
Iru79.3446.8979.3896.893
I-I7-v29.3406.8989.3976.894
I-I7-v39.3466.8989.3916.895
I-I7-v9.3426.8999.3946.894
I-Ü-3-d9.3476.8979.3836.893
I-Ü-3-v29.3446.8999.3886.893
I-Ü-3-v9.3446.8999.3866.892
Scanning electron microscopy (SEM) imaging and element mapping of polished valves embedded in PMMA resin were performed on a variable pressure Zeiss EVO MA15 SEM equipped with the Oxford X-MAX 80 energy dispersive detector system and Aztec Energy software for element analysis. For elemental mapping and analyses (EDS) the samples were carbon-coated. Carbon content was not measured. Elemental analysis was made according to shell lamination. Freshly broken surfaces of few selected specimens were coated with 5 nm thick Pt for inspection of crystallite morphology at higher magnifications on the same SEM instrument.
The Leica M205A optical microscope (OM) and SEM were used to select the regions of interest for ATR and EDS mapping. The shell areas with the most distinct lamination were chosen for mapping.
Polished cross sections of valves in PMMA, as well as powdered shell material of U. ingrica used for XRD analysis, are deposited at the Museum of Natural History, University of Tartu (TUG, Tartu Ülikooli Loodusmuuseum), in geological collection No. 1323. The shell of Lingula anatina that was used to compare the ATR-FTIR spectra is from the geological collections of the Institute of Geology at Tallinn University of Technology (GIT).

Results

XRD

Phase analysis of X-ray diffraction patterns revealed two apatite phases (referred to as A1 and A2 in Table , Fig. ) with distinct lattice parameter values in every valve studied. In addition, pyrite was detected as an accessory diagenetic phase.
Fig. 2. Graph of XRD data showing variations in lattice parameters a and c in Apatite 1 and Apatite 2 of Ungula ingrica (TUG 1323-5) and in modern Lingula anatina (Watabe & Pan ; LeGeros et al. ; Iijima & Moriwaki ; Iijima et al. ; Zezina et al. ; Puura & Nemliher ).

Microscopy

Optical microscopy (OM) and SEM imaging show a characteristic stratified nature of the shells with alternating compact and porous (baculate) laminae (Fig. A–F). Baculate shell structure (Fig. E) is poorly expressed in polished cross sections of shells (Fig. B,C), but can be occasionally revealed in SEM images in the internal parts of the shell (Fig. C). In most cases the shells appear massive under OM (Fig. A,B,F) and SEM (Fig. C,D). Shells are commonly pyritized (mainly shells from Iru, Fig. A) or hematized (mainly shells from Ülgase, Fig. F).
Fig. 3. (A–F), OM (A, B, F) and SEM (C, D, E) photos of Furongian Ungula ingrica. (A), TUG 1323-6, polished cross section of U. ingrica from Iru with white boxes showing the locations of IR mapping; The grey box shows the location of (B) and (C), this is also an area where EDS mapping (presented in Figure ) was conducted. (B), close-up of the grey box in A showing the alternation of compact (Cl) and baculate (Bl) laminae as they are seen under OM. (C), the same area as in (B), but under SEM; baculate laminae less filled with apatite can be seen in the lower parts of the shell; bright areas in the image are due to authigenic pyrite aggregates (Py); (D), TUG 1323-7, SEM image of an unpolished fracture section of a shell from Iru, the shell is tightly filled with apatite; the white box indicates the location of (E). (E), close-up of D showing a porous (baculate) lamina (Bl) between two compact laminae. (F), TUG 1323-8, polished hematized cross section of a shell from the Ülgase outcrop; White box indicates the area where IR mapping was conducted (Fig. E–F).
Elemental maps of shells of Ungula ingrica demonstrate a significant difference in the composition of compact and baculate laminae (Fig. ). Compared to baculate laminae, compact laminae are enriched in sodium and magnesium but depleted in calcium and fluorine. According to EDS elemental analyses, the two apatite varieties differ most clearly in their fluorine content, which is around 2–3 wt% in compact laminae and commonly more than 3.7 wt% in baculate laminae. The variations in other elements (Na, Mg, Ca) are less differentiated between the apatite phases in compact and baculate laminae. Both apatite phases contain more Na than Mg and the amount of either of the elements is <1 wt%.
Fig. 4. Results of EDS mapping of the polished cross section in Figure A (grey box). The shell was carbon-coated prior to mapping. The maps of Ca and F show higher concentrations in porous baculate laminae (wider, brighter) and lower ones in compact laminae (thin, dark laminae). The maps of Na and Mg show higher concentrations in thin compact laminae than in wide baculate laminae.

ATR-FTIR microspectroscopy

Representative ATR-FTIR spectra of Ungula ingrica shell apatite are shown in Figure . The spectra are similar to those of carbonated apatites, like the ones of fossil bone (Stathopoulou et al. ) or modern Lingula (LeGeros et al. ; Rohanizadeh & LeGeros ) and show characteristic absorption bands of PO43− and CO32− anions as well as OH/H2O groups.
Fig. 5. Representative ATR FT-IR spectra of modern Lingula anatina from the Philippines (GIT 587-32) and of the compact and porous (baculate) laminae of Furongian Ungula ingrica (TUG 1323-6). The spectra are shown in common scale. IR bands are sharper and better expressed in the fossil shell. Apatite 1 in porous laminae is richer in carbonate anions and has a characteristic strong ν2 C–O out-of-plane bending band in the CO32− anion at 864 cm−1, while three IR bands frequently appear in the ν2CO32− region in the apatite in compact laminae (Apatite 2). Apatite in compact laminae shows also a sharper P–O absorption band in the PO43− anion at about 1090 cm−1.
The most intensive IR bands are due to ν1 and ν3 P–O stretching vibrations of phosphate anions, PO43−, in the 1000–1100 cm−1 spectral range: ~964 cm−1 (ν1), ~1018 cm−1 (ν3) and ~1090 cm−1 (ν3). These phosphate bands are better expressed (sharper) in the spectra of fossil brachiopods (Fig. ) than in the spectrum of modern Lingula (Fig. ; see also fig. in Rohanizadeh & LeGeros ).
Carbonate substitution into the apatite crystal lattice results in the spectra of U. ingrica in a doublet band at about 1424 and 1455 cm−1 due to C–O asymmetric stretching vibration (ν3) in CO32− anion, and in two maxima at about 864 and 872 cm−1 with a weak shoulder at about 880 cm−1 due to C–O out-of-plane bending (ν2) in the CO32− anion (e.g. Fleet & Liu ).
In addition, we observed a weak broad band centred around 3400 cm−1 and a band at about 1630 cm−1. These are due to O–H stretching and bending vibrations, respectively, of molecular H2O, possibly adsorbed on sample surface (Elliott ).
A very weak (seen only in magnified spectra) but distinct band at around 3535 cm−1 (Fig. ) was identified as an O–H stretching band accompanied by a band at 749 cm−1 assigned to the O–H librational vibration mode (Dahm & Risnes ; Rintoul et al. ). In biological hydroxyapatites, the O–H stretching band occurs at somewhat higher wavenumbers (around 3570 cm−1) and shifts towards lower wavenumbers with increasing fluoride content and formation of hydrogen bonds between hydroxide and fluoride ions in apatite c-axis channels (e.g. Rodríguez-Lorenzo et al. ).
The third phosphate frequency region, ν4 PO43−, can only be seen partly (around the wavenumber 600 cm−1) because it occurs at the border of the detection limit of the MCT detector and ATR accessory with a Germanium crystal used for the IR measurements and can therefore not be used for further interpretations. The IR spectrum of the PMMA resin does not contribute much to the apatite bands (Lebon et al. ). The characteristic PMMA band at about 1730 cm−1 (C=O stretch) does not appear in the apatite spectra of the studied samples, indicating that PMMA has not infiltrated into the samples.
The ATR-FTIR spectra from compact and porous (baculate) laminae show distinct differences (Fig. ). The IR spectra obtained from porous laminae have higher carbonate absorption intensity than IR spectra in compact laminae. Increase in IR band intensities in the ν3 CO32− region is usually accompanied by the formation of an intense absorption band at the wavenumber 864 cm−1 in the ν2 CO32− region. With decreasing band intensities in the ν2 and ν3 CO32− regions three separate absorption bands with maxima at 872 cm−1 appear. The third change observable in IR spectra is the change in the intensity of the ν3 phosphate band at the wavenumber about 1090 cm−1 opposite to the intensity changes in carbonate regions. Higher absorption intensities in the ν2 and ν3 carbonate regions are accompanied by lower intensities at 1090 cm−1 and vice versa.
ATR mapping was focused on spatial distribution of ratios of carbonate and phosphate ion absorption band maxima and on the intensity ratios of the IR bands in the ν2 carbonate region. Infrared mapping analysis shows that spectral intensity changes have spatially distinct distribution and in the most conspicuous cases (Fig. A–G) the absorption intensity variations follow the stratiform microstructure of U. ingrica shells.
Fig. 6. (A–G), ATR FT-IR mapping of polished cross sections of Ungula ingrica shells from Iru (A–D, G; TUG 1323-6) and Ülgase (E–F; TUG 1323-8) outcrops. (A), ATR map (measured area 21 × 41 μm, step size 25 × 25 μm) from the ratio of C–O bending bands in the CO32− anion at 872 and 864 cm−1 showing a clear lamination; map area is shown on Figure A as the rightmost white box. B, the ratio map of P–O stretch in PO43− at 1091 cm−1 and C–O stretch in CO32− at 1429 cm−1 showing a less clear lamination, probably indicating that the diagenetic processes have not been uniform inside the laminae; the mapped area and mapping specifications are the same as in (A). (C), the ratio map (measured area 42 × 52 μm, step size 21 × 11 μm) of ν2 C–O bending bands in the CO32− anion at 864 and 871 cm−1 suggesting that the 864 cm−1 band is clearly in baculate laminae (higher intensities in red) and have very poor intensities (blue) in the central parts of compact laminae; map location is shown in Figure A with the central white box. (D), the ratio map of C–O stretch in CO32− at 1424 cm−1 and P–O stretching band in PO43− at 964 cm−1, indicating that the apatite in baculate laminae is rich in carbonate anions. Map location and mapping specifications are the same as for (C). (E), ratio map (measured area 30 × 40 μm, step size 7 × 7 μm) of the C–O stretch in CO32− at 1422 cm−1 and P–O stretching band in PO43− at 1090 cm−1 showing that the shell from Ülgase, although hematized, shows similar mapping results as the shell from Iru where carbonate intensities are higher in baculate laminae. Map location is shown in Figure F with the white box. (F), ratio map of a possible A-type carbonate (C–O) band 879 cm−1 and carbonate (C–O) band at 864 cm−1; map location and mapping specifications are the same as in E. G, ratio maps (measured areas 74 × 26 and 145 × 27 μm, step size 13 × 13 and 19 × 19 μm, respectively) of the P–O stretching band at 962 cm−1 and C–O stretching band at 1454 cm−1 showing clear lamination and that the apatite in zones cross-cutting shell lamination (marked with a triangle) has the same composition as the apatite in baculate laminae. The locations of the two maps are shown in Figure A with two white boxes on the left side of the shell. The maps have different intensity ranges.
The intensities of IR absorption bands as well as band positions vary in shell cross section across and also inside the laminae. Only in rare cases the IR intensities stay more or less constant. For example the 1091 cm−1/1429 cm−1 absorption ratio map (Fig. B) shows lower values in two middle baculate laminae than in other baculate laminae. In general, the ratios of ν2 carbonate region band intensities show better expressed lamination (Fig. A,C,F) than the ratios of carbonate and phosphate bands (Fig. B,D,E,G).
The carbonate 1450 cm−1 and phosphate 960–1000 cm−1 band ratio, though distinctly different between laminae, does not show significant variation within porous and compact lamina. Exceptions are occasional 50–150 μm wide zones/pockets cross-cutting the original stratiform structure of the shells (Fig. G, marked with a triangle). These zones are visible also in OM (e.g. Fig. A below the leftmost white box) and SEM backscatter images and are characterized by the apatite composition similar to that in porous laminae.

Discussion

Our results show that valves of the Cambrian linguliform brachiopod U. ingrica are composed of two distinct apatite phases. Their distribution within the shell correlates well with the original shell structure. We refer to these phases as Apatite 1 and Apatite 2.

Apatite composition and distribution

Apatites, Ca5(PO4)3(F,OH,Cl), have a very variable composition, due to diverse chemical substitutions (Hughes & Rakovan ). Calcium in the apatite crystal lattice could be substituted by other cations, for example Na+ or Mg2+, the phosphate anion is most frequently partly substituted by carbonate (CO32−), and the channel anions OH and F are most commonly substituting for each other or Cl (Pan & Fleet ). Carbonate ion can be located in apatite structure either in the structural channel along the crystallographic c-axis (referred to as A-type carbonate) or as a substituent for PO4 (B-type carbonate) (Elliott ). Due to all these substitutions, various types of apatite can be differentiated by their unit cell dimensions, elemental and anionic composition.
The ATR-FTIR analyses suggest that Apatite 1 which is found in porous (baculate) laminae is characterized by a higher content of the carbonate ion, expressed in the intensity ratios of C–O/P–O bands (Fig. D,E). The decreased resolution of the ν3 P–O band in PO43− at 1092 cm−1 (Fig. ) could also be explained with the increased carbonate content (Antonakos et al. ). The ν2 carbonate vibration in Apatite 1 (in baculate laminae) has a strong C–O bending band at 864 cm−1 and the apatite composition is depleted with respect to PO43−, Mg and Na, and enriched with F and Ca (Figs  and ) in comparison with that in compact laminae. The band at around 864 cm−1 in bioapatites has been ascribed to a labile/unstable carbonate species which is not assigned to A or B sites and is possibly located on the crystal surfaces (e.g. Rey et al. ), while bands at 872 cm−1 and 880 cm−1 are attributed to B- and A-type carbonate substitutions, respectively (Elliott ). However, in carbonate-fluor apatites (francolites) the 872 cm−1 and 880 cm−1 bands are shifted to 864 cm−1 and about 876 cm−1, respectively (e.g. Regnier et al. ; Antonakos et al. ). Additionally, Fleet shows the presence of two B-type carbonate sites in Na-containing francolite – B2 at about 865 cm−1 and B1 at 873 cm−1, and an A-type carbonate ion vibration band at 881 cm−1. One of the possible explanations is that the B2 band represents a B-type carbonate not coupled with the A-type channel carbonate ion, which could be achieved if the channel sites are essentially all occupied by fluorine (Fleet ). Yi et al., on the other hand, explain the appearance of the 864 cm−1 band by the formation of the so-called francolite-type defect where carbonate together with the fluoride ion replaces the tetrahedral phosphate ion in the apatite structure. They suggest that the appearance of this band (864 cm−1) could be used as a guide to diagenetic changes in fossil teeth and bones as this band has been reported from fossil skeletal fragments (e.g. Stathopoulou et al. ). In our samples, the apatite in porous laminae is characterized by an increased F content compared to the apatite in compact laminae (Fig. ). Thus, the high fluoride content and/or specific crystallo-chemical changes in fossil apatite could explain the presence of a strong B2-type carbonate absorption band at 864 cm−1 in this apatite phase.
In Apatite 2 that forms compact laminae, Ca is substituted by Na and Mg and the concentration of F is lower than in Apatite 1 (in baculate laminae) (Fig. ). The ATR-FTIR spectrum of Apatite 2 revealed relatively lower absorption intensities of bands in the ν2 and ν3 CO32− regions, suggesting a relatively lower carbonate anion content (Figs  and B,D,E,G). This phase is additionally characterized by the appearance of the B-type (i.e. phosphate replacing) carbonate band at 872 cm−1 (Figs  and A,C). The band near 872 cm−1 is typically the strongest ν2 carbonate band for recent bioapatite in bones (Elliott ), modern Lingula (LeGeros et al. ; Rohanizadeh & LeGeros ) and synthetic carbonate-OH-apatite (Antonakos et al. ). Moreover, the FTIR spectra of Apatite 2 in U. ingrica shells suggest that besides prevailing B-type (B1-type) carbonate substitution, some A-type carbonate substitution may also be present. This is indicated by the higher intensity of the 880 cm−1 absorption band in compact laminae in the ATR map of the ν2 carbonate bands (Fig. F) and by a weak shoulder appearing in the ν2 carbonate region at about 880 cm−1 in Apatite 2 (in compact laminae) spectra (Fig. ).
Different elemental and anionic composition of apatite phases revealed by ATR-FTIR and SEM-EDS analysis allows tentative coupling of these apatites to the two phases with different unit cell dimensions as evident from XRD analysis. The substitution of carbonate for the phosphate anion and fluoride for the OH in channel sites of the apatite crystal lattice are typically considered as having a diminishing effect on apatite unit cell dimensions along the a-axis direction (Elliott ; Yao et al. ). Therefore, Apatite 1 with elevated F and carbonate concentration in porous baculate laminae is most probably the phase characterized by lower values of lattice parameter a varying between 9.340 and 9.347 Å (Table , Fig. ). Consequently, Apatite 2 with higher parameter a values varying between 9.377 and 9.397 Å constitutes the compact laminae of the shell. Our results agree with interpretation by Nemliher et al. that higher XRD lattice parameter a values could be associated with the phase in compact laminae and represent the primary (skeletal) apatite. On the other hand, the reason for higher lattice parameter values of Apatite 2 could lie in the occurrence of OH or CO32− (A-type carbonate substitution) in the apatite structural channel sites. Though FTIR data suggest that some of A-type carbonate substitution may be present and more intensive in Apatite 2 (in compact laminae), it is not missing from Apatite 1 (in baculate laminae) either. The intensity of the O–H absorption band in the ATR-FTIR spectra of the studied samples is very weak and does not give any spatial variation in ATR maps, thus OH substitution could not explain the shift in unit cell parameters. However, the presence of O–H bands has been suggested for apatite in modern lingulates (LeGeros et al. ; Puura & Nemliher ; Rohanizadeh & LeGeros ) and for Cambrian Obolus apollinis Eichwald (Nemliher et al. ). O–H absorption bands have been detected in Estonian Cambrian – Ordovician shelly phosphorite samples calcined at high temperatures (Veiderma & Knoubovets ) and from the shells of modern Lingula heated in air (but not in N2) to temperatures higher than 700 °C (Iijima et al. ). It has been suggested that the appearance of O–H bands at about 3535 and 749 cm−1 in calcined phosphate spectra indicates the high F content of the sample (e.g. Rodríguez-Lorenzo et al. ). Nevertheless, it must also be considered that different substitutions (e.g. Cl and CO32−, the presence of HPO42− or H2O in apatite structure) may cancel each other and the interpretation of unit cell parameters is not straightforward (Elliott ).

Implications for diagenetic recrystallization and preservation

The crystallochemical characteristics (Fig. ) and chemical composition of Ungula ingrica apatite phases significantly differ from these of the skeletal mineral of modern linguliform brachiopods. These differences are most probably related to diagenetic recrystallization of original bioapatite. Bioapatite of modern linguliform brachiopods is a CO32− and F-containing OH-apatite that is crystallochemically similar, but not identical to francolite (LeGeros et al. ; Puura & Nemliher ). Forchielli et al. report that the shell composition as well as microstructure of modern Lingula show no significant variation within species due to geographical and environmental factors, though the number of phosphatic laminae varies between different genera and between species in the same genus. Shell chemistry of different brachiopod genera can be somewhat varying. For example, Glottidia shell apatite has been reported to have higher carbonate content than the shell apatite of Lingula, whereas the general F content is similar for both species (LeGeros et al. ). Several studies have, however, noticed that F content varies between shell laminae. LeGeros et al. show that the average F content is around 2.6 wt% in Lingula and Glottidia, and is higher in the highly calcified exterior laminae than in the internal laminae. On the contrary, the results of WDS (wavelength dispersive spectroscopy) microprobe analyses of the modern Lingula anatina shell by Forchielli et al. show fluorine values around 2.6 wt% for the external laminae and 3.5 wt% for the internal laminae.
Post-mortem alteration of bioapatite is principally driven by thermodynamic disequilibrium between biologically secreted mineral and the surrounding (geochemical) environment. Biominerals, typically grown from an amorphous precursor, have a relatively high degree of structural disorder that will be stabilized via dissolution/recrystallization of unstable primary phases and precipitation of phases in (quasi)equilibrium with the environment, or growth of new authigenic phases (e.g. Trueman ). These processes are usually accompanied by dissolution of nanometre-scale disordered small crystallites and growth of larger micrometre-scale crystals. Moreover, in addition to recrystallization of existing bioapatite, some secondary apatite could have been precipitated through bacterially mediated processes driven by sulphate-reducing bacteria degrading the organic tissues of the lingulates under suboxic to anoxic conditions (Lécuyer et al. ) as suggested by common digenetic pyrite mineralization within the laminar structure of studied brachiopod shells (Fig. C).
It is evident that Apatite 1 in porous baculate laminae of U. ingrica represents mainly an authigenic phase. The baculate laminae in living lingulate brachiopods are rich in organics, a substantial amount of which is in fibrous form (e.g. Iwata ; Williams & Cusack ; Merkel et al. ; Schmahl et al. ). Baculate sets similar to Ungula have been described for example in a living brachiopod Discinisca tenuis (Sowerby), where organic laminae consist of biopolymers, such as glycosaminoglycans and chitin fibrils (Williams et al. ; Williams & Cusack ). During post-mortem processes, labile organics is the first that starts to degrade, inducing the growth in porosity of baculate laminae, where pore fluids of various origin could circulate. Mineral-reinforced organic fibrous frameworks within the organic matrix, however, appear to be more resistant to decay and may stay in the organic laminae for a prolonged time. Therefore, it could be possible that some of the original fibrous network was preserved in the shells of U.ingrica and offered a template for the authigenic apatite to nucleate. Indeed, previous studies on Cambrian (Furongian) linguloid brachiopods Obolus ruchini and Ungula inornata (Lang et al. ; Lang & Puura ) have shown that phosphatized fibrous networks are preserved with various fidelity in baculate laminae, depending possibly on the nature of early diagenetic processes.
The XRD lattice parameters that could be associated with Apatite 1 (in baculate laminae) show values typical of carbonate-rich fluorapatites of marine origin (McClellan & van Kauwenbergh ). Lattice parameter values of this phase are also less varying than for Apatite 2 (in compact laminae) (Fig. ), suggesting similar conditions for apatite precipitation in different brachiopod valves and locations. The influence of the different localities on unit-cell lattice parameter values of diagenetically replaced apatite has been documented before (e.g. Stathopoulou et al. ). However, the specific locations considered in this study (Iru and Ülgase) cannot be differentiated on the basis of lattice parameter values, probably due to the small distance between these outcrops (only about 10 km).
Secondary origin of Apatite 1 in baculate laminae is further supported by its elevated F and carbonate contents. The solubility of apatite increases significantly with the increasing carbonate content of apatite and at the seawater phosphate concentrations the equilibrium solubility of carbonate fluorapatite is two orders of magnitude greater than it would be in equilibrium with pure fluorapatite (Jahnke ). However, fluorapatite of a relatively high carbonate content, as observed in baculate laminae, is possibly the thermodynamically stable apatite phase in solutions with elevated (bi-)carbonate anion activity such as seawater (Jahnke ).
Contrary with authigenic F-rich carbonate apatite composing baculate laminae we interpret Apatite 2 in compact laminae as a skeletal, but diagenetically modified apatite. No living representative is known for the obolids (family Obolidae) to whom also U. ingrica is assigned (Holmer & Popov ). Therefore, we can only speculate to which extent the primary characteristics of shell apatite could have been preserved in U. ingrica compact laminae. In analogy with tooth enamel of vertebrates that is usually better preserved than dentine (e.g. review by Brand et al. ), apatite can be better preserved in compact laminae than in baculate laminae because of the tighter arrangement of apatite crystals in compact laminae (Cusack & Williams ). Porous baculate laminae are composed of elongated >1000 nm long and >100 nm in diameter prismatic crystallites, whilst compact laminae consist of subhedral apatite granules of about 50 nm in size (Fig. ). Compact laminae of living brachiopods are formed of tightly packed spheroidal apatite particles about 50 nm in diameter and enmeshed in chitin fibrils (Schmahl et al. ). This similarity between apatite crystal sizes in fossil and living brachiopods suggests that, at least from the crystal size perspective, the compact laminae of the best preserved specimens of Furongian U. ingrica have not much changed. This could be explained by crystallochemical (meta)stability of the skeletal apatite of linguliform brachiopods. First of all, the original brachiopod apatite is a carbonate-fluor apatite-like mineral (francolite), whereas the vertebrate bioapatite is a hydroxyapatite-like poorly crystalline phase (Neary et al. ). The latter is thermodynamically unstable and is diagenetically readily recrystallized, while the carbonate-fluor apatite is a common stable sedimentary apatite (Jahnke ; McClellan & van Kauwenbergh ; Knudsen & Gunter ). Apatite secretion in linguliform shells, being directed, but not actively controlled by organic matrix-mineral interaction as in vertebrate tissues, results in precipitation of an already well-crystalline francolite-like mineral (Neary et al. ). In vitro formation of francolite from an amorphous precursor is possibly promoted by proteins in the brachiopod shell (Lévêque et al. ). The compact laminae of the linguliform brachiopod shell are thus composed of an already (more) stable mineral phase.
Fig. 7. Ungula ingrica (TUG 1323-9) from the Iru outcrop, non-polished fracture section, coated with 5 nm thick Pt for conductivity. SEM (secondary electron) photo of the mineral forms composing the compact (Cl) and porous baculate (Bl) laminae. Apatite particles in compact laminae are around 50 nm in size, but much larger in porous baculate laminae.
The lattice parameter values are more variable in Apatite 2 (in compact laminae) than in Apatite 1 (in baculate laminae) (Fig. ), seemingly resembling the behaviour of the widely varying lattice parameter values of modern Lingula anatina (Fig. ). However, in fossil shells such variation could also be caused by diagenetic changes affecting individual shells differently.
According to EDS analyses the fluorine content seems not to have changed much, but the differences in elemental composition other than F between Apatite 1 (in baculate laminae) and Apatite 2 (in compact laminae) are only slight. Moreover, the shell apatite of modern Lingula contains more Mg than Na (Forchielli et al. ), which is opposite to the apatite phases in fossil Ungula. These differences suggest that shell apatite has probably been somewhat altered. It is suggested that the alteration of shell apatite starts already at brachiopod lifetime (LeGeros et al. ; Puura & Nemliher ). Rapid alteration and/or vital effects of linguliform brachiopod apatite composition are also suggested by largely variable δ18OPO4 composition of phosphate in modern species, which complicates the application of oxygen isotope composition in biogenic phosphates for reconstruction of palaeoenvironments as a palaeothermometer (Rodland et al. ). Goldhammer et al. shows that the enzymatic regeneration of P from organic matter produces distinct offsets from equilibrium with water, meaning that secondary apatite (Apatite 1) in baculate laminae is not suitable target for palaeoenvironmental information. Interference of a secondary, bacterially influenced, apatite would also explain why the estimated palaeotemperatures inferred from phosphate oxygen isotope analyses of lingulate brachiopods (Lécuyer et al. ; Elrick et al. ) are much higher than expected. Similar recrystallization/authigenesis processes could also influence the paleothermometric usability of phosphate oxygen isotope composition of Cambrian - Early Ordovician conodonts, typically enriched with organic material (Szaniawski & Bengtson ).
The time scales and intensity of these changes are difficult to assess at this point, but since; 1, the overall post-mortem compositional change of the apatite in compact laminae of linguliform brachiopods is rather limited; 2, baculate laminae show at least partial preservation of delicate mineralized organic fibrous frameworks (Lang & Puura ) and 3, shell laminae contain authigenic pyrite (Lécuyer et al. ) suggesting alteration mediated by sulphate-reducing bacteria that commonly thrive in the uppermost few-tens of centimetres thick sediment column at the sea bottom (Jørgensen ), then it is possibly a rapid early diagenetic phenomenon.

Conclusions

The shells of Cambrian Ungula ingrica showed clear laminated alternation of apatite phases with different chemical compositions. These phases can be associated with compact (Apatite 2) and baculate (Apatite 1) laminae in brachiopod shell structure.
The apatite phases revealed in brachiopod shells have different origin. Chemical differences between them are most clearly expressed in the content of fluorine and carbonate ions in the apatite crystal lattice, whereas the changes at cationic sites are less pronounced. The apatite phase that is associated with porous baculate laminae (Apatite 1) is mostly composed of authigenic apatite. This phase is characterized by a higher fluorine and carbonate content and its cationic sites are mainly occupied by Ca. The high fluorine and carbonate content likely causes the lower XRD lattice parameter values for this phase.
The apatite phase associated with compact laminae (Apatite 2) can be interpreted as early diagenetically recrystallized skeletal apatite, which may have preserved some of its original characteristics. This phase has the F content, crystal size and lattice parameter a values similar to the apatite in modern brachiopod shells. It also contains less carbonate than the authigenic apatite phase. However, the differences in cationic substitutions between the skeletal and authigenic apatite in the studied fossil brachiopod shells are only slight. Thus, based on combined results of FTIR microscopy in the ATR mode and EDS we may conclude that if there are some original features of shell apatite preserved, these can most probably be found in the (central parts of) compact laminae. Nevertheless, compared to modern linguliform brachiopods, unit-cell dimensions of the apatite mineral in compact laminae, if correctly interpreted, show a significant diagenetic rearrangement in the crystal structure.

Acknowledgements

We thank Lauri Joosu for help with SEM studies and Jaan Aruväli for making the XRD analyses. Ursula Toom from the Institute of Geology at Tallinn University of Technology is acknowledged for providing the shell of modern Lingula anatina for study. Tõnu Meidla and Giuseppe Buono are thanked for the useful comments, suggestions and discussions during various stages of writing this article. We are grateful to the two reviewers who helped us to improve the manuscript. The support of Estonian Science Foundation grant No. 8049 ‘Biotic recovery events in the Ordovician and Silurian’ and from the Estonian Research Agency IUT20-34 ‘The Phanerozoic journey of Baltica: sedimentary, geochemical and biotic signature of changing environment – PalaeoBaltica’ are acknowledged.

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Volume 49Number 11 January 2016
Pages: 1327

History

Received: 18 March 2014
Accepted: 10 November 2014
Published online: 6 March 2015
Issue date: 1 January 2016

Authors

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Department of Geology, University of Tartu, Ravila 14A, Tartu, 50411, Estonia;
Kalle Kirsimäe [email protected]
Department of Geology, University of Tartu, Ravila 14A, Tartu, 50411, Estonia;
Signe Vahur [email protected]
Institute of Chemistry, University of Tartu, Ravila 14A, Tartu, 50411, Estonia;

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