Fujioka et al. Progress in Earth and Planetary Science
https://doi.org/10.1186/s40645-019-0289-7(2019) 6:45

RESEARCH ARTICLE

Progress in Earth andPlanetary Science

Open Access

The effects of meteoric diagenesis on thegeochemical composition andmicrostructure of Pliocene fossil
Terebratalia coreanica and Laqueus rubellus
brachiopod shells from northeastern Japan
Hiroshi Fujioka1, Hideko Takayanagi1, Koshi Yamamoto2 and Yasufumi Iryu1*

Abstract
Stable carbon (δ13C) and oxygen isotope (δ18O) compositions of fossil brachiopod shells can be used to interpret
paleoclimatic and paleoceanographic conditions. However, the initial isotopic composition of the living shells might
be modified by diagenetic alteration. To assess the degree of this modification, we analyzed δ13C and δ18O andthree common indicators of alteration in shells: minor element (manganese (Mn), iron (Fe), and strontium (Sr))
concentrations; cathodoluminescence (CL)/non-luminescence; and the shell microstructure of fossil Terebratalia
coreanica and Laqueus rubellus (rhynchonellate brachiopod) shells from an exposure of conglomerates of the
Tentokuji Formation (Pliocene, 3.85–2.75 Ma) in northeastern Japan. Two indices were used to quantify thepreservation state of shell microstructure: the altered fiber ratio (AFR) and the altered fiber and puncta-fillingcement ratio (AF-PCR). We qualified the degree of luminescence by measuring the mean cathodoluminescenceindex (MCLI), defined as the mean R values in a particular area of a CL image with RGB colors. The δ13C and δ18O
values were negatively correlated with AFR or AF-PCR and MCLI. The sampling spots with high Mn and Fe
concentrations also exhibited relatively low δ13C and δ18O. The δ13C and δ18O were more strongly correlated with
Mn concentration than with Fe concentration. Therefore, of the three minor elements examined in this study, Mnconcentration is the most reliable indicator of meteoric diagenesis in the studied shells. Unlike Mn and Fe
concentrations, Sr concentrations in the modern and fossil brachiopod shells were similar, with overlapping ranges.
This indicates that Sr concentration is not likely to be a good indicator of diagenetic alteration in the studied shells.
Our study provides further evidence that multiple criteria should be applied and cross-checked when assessing
diagenetic alteration of brachiopod shells.
Keywords: Brachiopod, Carbon isotopes, Oxygen isotopes, Minor element concentration, Cathodoluminescence,
Meteoric diagenesis, Terebratalia coreanica, Laqueus rubellus, Pliocene, Japan* Correspondence: yasufumi.iryu.d8@tohoku.ac.jp
1
Department of Earth Science, Graduate School of Science, Tohoku
University, Sendai 980-8578, Japan
Full list of author information is available at the end of the article© The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, andreproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made.

(2019) 6:45

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Introduction
Stable carbon isotope (δ13C) and oxygen isotope (δ18O)
compositions of biogenic carbonates are useful for
paleoenvironmental analysis. The δ13C and δ18O values ofshells from brachiopods belonging to the subphylum
Rhynchonelliformea (Williams et al. 1996; hereafter, simply called brachiopods) have been widely used for reconstructing paleoclimatic and paleoceanographic conditions
during the Phanerozoic, and especially during the
Paleozoic (e.g., Veizer et al. 1999), because of (1) theirwidespread occurrence in marine sediment and their continuous geologic record; (2) their low-magnesium calcite
mineralogy, which is less susceptible to diagenetic alteration than high-magnesium calcite and aragonite; and (3)shell secretion in isotopic equilibrium with ambient seawater (Lowenstam 1961). The disequilibrium effects ofshell fractionation have been very well investigated since
Lowenstam (1961), and it is understood in detail which
taxa and shell portions reliably record past ocean environments with the highest fidelity (Auclair et al. 2003; Yamamoto et al. 2010a, 2010b, 2011, 2013; Cusack et al. 2012;
Takayanagi et al. 2012, 2013, 2015).
To evaluate the preservation of brachiopod shells, thefollowing three screening criteria have been commonly
applied (Ullmann and Korte 2015): (1) minor element(manganese (Mn), iron (Fe), and strontium (Sr)) concentrations, which vary with diagenetic alteration; (2) luminescence/non-luminescence with “cold cathode”; and (3)shell microstructures observed via scanning electron
microscope (SEM). Well-preserved shells or shell portions
are non-luminescent, having high Sr and low Mn and Fe
concentrations and well-preserved microstructure.
However, these techniques do not work effectively inall cases. It has been shown that there might be no significant difference in the isotopic composition between
well-preserved and diagenetically altered shells determined using the minor element concentrations (e.g.,
Bruckschen et al. 1999; Korte et al. 2005). Some unaltered modern brachiopod shells show bright cathodoluminescence (CL) images (e.g., Barbin and Gaspard
1995; Griesshaber et al. 2007), which is usually taken to
be an indication of diagenetic alteration. The δ13C andδ18O values of luminescent and non-luminescent shells
might overlap or be similar in range (Rush and Chafetz
1990; Mii et al. 1997, 2013; Yamamoto et al. 2017).
Therefore, applying multiple criteria to assess the diagenetic alteration and cross-checking them are required
to distinguish between diagenetically altered and unaltered brachiopod shells (Yamamoto et al. 2017).
The isotopic and minor element signatures in carbonate
minerals vary with the isotopic and chemical compositionof the ambient pore water (Wenzel 2000; Ullmann et al.
2014), which can be marine, meteoric, or hydrothermal
water, or various mixtures of these. This variation implies

that diagenetic modification of the chemical and isotopic
composition in brachiopod shells embedded in carbonate
deposits is likely to be different from that in siliciclastic
and volcaniclastic deposits. Cathodoluminescence imagesof brachiopod carbonates might not be useful for detecting diagenetic alteration where sources of Mn (the activator for CL) are very limited. There are some instances
showing that the δ13C and δ18O values or the preservationof shell microstructure are unrelated with CL intensity(Yamamoto et al. 2017).
To better understand the impact of diagenetic modification on the isotopic and chemical composition of brachiopod shells in siliciclastic deposits, we examined theδ13C and δ18O values, minor element concentrations,
CL images, and shell microstructure of fossil brachiopod
shells of two species, Terebratalia coreanica (Adams andReeve 1850) (Family Terebrataliidae Richardson 1975)
and Laqueus rubellus (Sowerby 1846) (Family Laqueidae
Thomson 1927) collected from the conglomerates of the
Pliocene Tentokuji Formation in Minehama, northeastern Japan. We compared these shells with modern shells
from Otsuchi Bay (northeastern Japan) and Sagami Bay(central Japan). Terebratalia coreanica is generally foundat water depths of 13–287 m in the northwestern Pacific
Ocean (Hokkaido, Tsugaru Strait to Boso Peninsula on
the Pacific side, Korean Strait north to Tsugaru Strait on
the Japan Sea side, Japan; Tsingtao, China; Korea; andthe Gulf of Tartary, Russia) (Hatai 1936a, 1936b, 1938;
Logan 2007). Laqueus rubellus inhabits water depths of
44–907 m in the Pacific Ocean (the seas around Japan;
the Japan Sea; Pailolo channel, Hawaii) (Dall 1920; Hatai
1936a; Logan 2007). The wide spatiotemporal distribution of these species means that their δ13C and δ18O
values are potentially useful for reconstructing the paleoceanographic environments of lower sublittoral to upper
bathyal zones during the late Mesozoic to Cenozoic.

Fujioka et al. Progress in Earth and Planetary Science

Materials and sample sites
Modern specimens
Terebratalia coreanica from Otsuchi Bay

Modern T. coreanica (OTTCo; Fig. 1a) were collectedby dredging at 70 m water depth in Otsuchi Bay (39°21.86′ N, 141° 59.97′ E) along the Sanriku Ria Coast in
northeastern Japan, using the research vessel Yayoi of
the International Coastal Research Center, Atmosphereand Ocean Research Institute (ICRS/AORI), The University of Tokyo, on 12 September 2005. Highresolution, three-dimensional δ13C and δ18O values ofthis species have been published by Yamamoto et al.
(2011, 2013). The δ13C and δ18O values of calcite precipitated in isotopic equilibrium with ambient seawater(equilibrium calcite) at the brachiopod collection siteranged from 1.4 to 2.6‰ (δ13CEC) and from − 1.4 to
2.4‰ (δ18OEC) (Yamamoto et al. 2011, 2013). The

(2019) 6:45

Fujioka et al. Progress in Earth and Planetary ScienceaPage 3 of 23bc

MNTCo1
MNT

OTTC
OTTCo

e

d

MNTCo2f

MNTCo3
3
MNTCo4ghj

MNTCo5

i

SGLR

MNLR1

k

l

MNLR2

2 cm

MNLR3

MNLR4

MNLR5

Fig. 1 Photographs of the Terebratalia coreanica and Laqueus rubellus shells examined in this study. The modern T. coreanica shells were collectedfrom Otsuchi Bay, northeastern Japan, and L. rubellus shells were collected from Sagami Bay, central Japan. The fossil shells are from the Pliocene
Tentokuji Formation in Minehama, northeastern Japan. a Modern T. coreanica. b–f Fossil T. coreanica. g Modern L. rubellus. h–l Fossil L. rubellus.
Only the ventral valves were examined in this study

δ13CEC values were calculated by using the δ13C valuesof inorganic carbon (DIC) at the brachiopod collection
site (Otsuchi Bay), the difference between δ13CHCO3−
and 13CDIC values (0.2‰, Grossman 1984, Romanek et
al. 1992, Zhang et al. 1995), and the calcite-HCO3− enrichment factor (1.0 ± 0.20‰, Romanek et al. 1992)(Additional file 7: Doc. S1). The δ18OEC values were estimated based on the equation given by Friedman andO’Neil (1977) (Additional file 7: Doc. S1).
Laqueus rubellus from Sagami Bay

Modern L. rubellus (SGLR; Fig. 1g) were collected by
dredging at 80 m water depth at the eastern margin of
Sagami Bay, central Japan (35° 08.17′ N, 139° 34.86′ E),
during a cruise of the fishing vessel Rinkai-maru, basedat the Misaki Marine Biological Station, The Universityof Tokyo, on 16 June 2005. Yamamoto et al. (2010a)
have presented high-resolution, three-dimensional δ13C
and δ18O values of this species. The δ13CEC values
ranged from 1.6 to 2.6‰, and δ18OEC ranged from − 0.6
to 0.8‰ (Yamamoto et al. 2010a). These values were calculated by the same method as described above.
Fossil shells

Fossil T. coreanica (MNTCo1–MNTCo5; Fig. 1b–f ) andL. rubellus (MNLR1–MNLR5; Fig. 1h–l) were collectedfrom sandy conglomerates of the upper part of the Pliocene Tentokuji Formation exposed at Minehama (MH1,Amano et al. 2011), Happo-cho, Akita Prefecture, northeastern Japan (Fig. 2; 40° 17.18′ N, 140° 4.52′ E). The

Fujioka et al. Progress in Earth and Planetary Science(2019) 6:45

Page 4 of 23ab

HokkaidocMinehama

Yoneshiro River

Noshiro

b
40°N

Akita

Oga

Terrace Deposit

gravel & sandSasaoka F.

very fine–
fine sandstone

Tentokuji F.

140°E

fa
ul
t

Sendaicalternation of siltstone& conglomerate
sandy siltstone–siltstone
pumice tuff

Funakawa F.
mudstone

Onnagawa F.

hard mudstone

Hanawa
r
ive
R
a
aw
n
Ha

Sampling site

0

1 km

Fig. 2 Location and geologic map of the sample site. a Akita Prefecture, northeastern Japan. b Enlarged view of the square in a. c Geologic mapof the Minehama area (modified from Sato et al. 2003). The red star indicates the site at which the fossil Terebratalia coreanica and Laqueus
rubellus shells were collectedhorizon with the fossil brachiopod shells is dated 3.85–
2.75 Ma, owing to its location between the Upper Pliocene datum planes (datum planes 21 and A) (Sato et al.
2003), which represent ages of 3.85 Ma and 2.75 Ma(Sato and Kameo 1996).
The Upper Miocene to Pleistocene succession around
Minehama consists of the Onnagawa, Funakawa, Tentokuji, and Sasaoka formations in ascending order (Fig. 2c;Sato et al. 2003). The Onnagawa Formation is composed
mainly of hard mudstone (generally termed “hard shale”)

conformably overlain by the Funakawa Formation, which
comprises mostly mudstone and pumice tuff. The Tentokuji Formation, conformably overlying the Funakawa
Formation, consists mainly of dark bluish-gray siltstonealternating with conglomerates in the middle-upper intervals of the formation. The alternating beds are
regarded as a turbidite sequence (Sato et al. 2003). The
conglomerates yielding the brachiopod shells analyzed in
the present study are 5–10 cm thick and consist ofrounded to sub-rounded, granule to pebble-sized gravel(2019) 6:45

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of andesite and, to a lesser extent, pumice, with a matrix
of coarse-grained volcaniclastic sand. The Sasaoka Formation conformably overlies the Tentokuji Formationand consists of poorly sorted, very coarse to coarsegrained sandstone. Bivalves that co-occur with the brachiopods indicate a lower sublittoral zone depositional
environment (Higo et al. 1999; Amano et al. 2011).

(e.g., Angiolini et al. 2007; Garbelli et al. 2014, 2016; Takizawa et al. 2017). This procedure yields a relatively narrow
range of δ13C and δ18O values because of the minimal
fractionation effect in this region of the shell, arising fromthe very low growth (shell thickening) rate, except in andaround specialized shell portions (e.g., muscle scars andthe foramen).
Ventral valves of the brachiopod shells were embedded
in a resin epoxy matrix and vertically cut along the maximum growth axis (Fig. 3) with a 0.4 mm thick IsoMet
low-speed saw (Buehler, Lake Bluff ). The samples forisotopic and minor element analyses (~ 0.1 mg for eachanalysis) were obtained from locations within 0.5 mm ofthe inner shell surface at 1 mm intervals (red arrows in
Fig. 3) in a thick (> 1 mm) shell portion using a 0.2 mm
diameter drill and at 2 mm intervals (blue arrows in
Fig. 3) in a thin (< 1 mm) shell portion with a 0.10–
0.12 mm diameter drill. The sampled spots were ~ 0.6–
2.3 mm in length and less than 0.5 mm wide. We used a
diamond-coated drill bit for extracting samples to prevent contamination by iron present in the drill bits.
Individual shells were divided into three intervals
based on the shell morphology: interval 1 corresponding

Fujioka et al. Progress in Earth and Planetary Science

Methods/Experimental
High-resolution microsampling

The δ13C and δ18O values of the modern brachiopod
shells display significant intra-shell, intra-species, andinter-species variations, and the isotope composition is
not in all cases within the range of values of equilibrium
calcite (Auclair et al. 2003; Yamamoto et al. 2010a, 2010b,
2011, 2013; Cusack et al. 2012; Takayanagi et al. 2012,2013, 2015). Therefore, specific shell portions, for whichthe δ13C and δ18O values are identical to the δ13CEC andδ18OEC values, respectively, must be selected when using
the isotopic signatures as paleoenvironmental proxies.
Therefore, in recent studies, samples have been extracted
from spot locations on the inner shell surfaces in verticalsections along the maximum growth (longitudinal) axis
Isotope analysis

Maximum growth axis

Cut

Primary layer

Minor element analysis

Transverse
section

SEM

Ventral valve

Secondary layer
2 mmAnteriorshell edge

diam

eter

1m

m

Sampling spot

dia

me

ter

Cathode-Luminescenceobservation

Dorsal valve

ventral median ridge (VMR)

posteriorshell edge

Interval 1

Interval 2Interval 3

anteriorshell edge

Fig. 3 Schematic illustration of the sampling procedure for geochemical analyses of the modern and fossil shells. The red and blue arrows
indicate sampling intervals of 1 and 2 mm, respectively. Shells were cut along the maximum growth line and then along a line perpendicular to
the maximum growth axis. Thin sections along the maximum growth axis were examined in CL images. SEM observations were carried out on
the cross-section along the line perpendicular to the maximum growth axis. Individual shells were divided into three intervals (intervals 1–3)
based on the shell morphology

(2019) 6:45

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to a thick posterior shell region, interval 2 located between intervals 1 and 3, and interval 3 denoting the thinanterior shell region (Fig. 3). This division is identical tothat proposed for Kikaithyris hanzawai shells (Takizawa
et al. 2017). The boundary between intervals 1 and 2 inboth species corresponded to a convex portion locatedin the center of ventral valves, which was identical to
the “ventral median ridge (VMR)” reported from theventral valves of K. hanzawai (Endo 1989), and hereafter,
we use this term. The VMR was located 12.5–16.3 mmfrom the posterior shell edge in T. coreanica and 13.2–
14.6 mm in L. rubellus. The boundary between intervals 2
and 3 was a region where the shell thickness became lessthan 1 mm. This region was located 4.6–12.8 and 3.8–
10.2 mm from the VMR toward the anterior shell edge inT. coreanica shells and L. rubellus shells, respectively.
Powder samples were extracted from calcite cement in
an internal cavity (7 mm × 4 mm in diameter) of a fossil
brachiopod shell using the same method as describedabove. This brachiopod shell was small (a distance fromthe posterior shell edge to the anterior shell edge of < 1cm) and was not used for geochemical analyses in thisstudy. The inner shell surface of the fossil brachiopod
was covered thinly with blocky equant calcites with undulated protuberances (~ 2 mm long and ~ 1 mm indiameter) showing a helictite-like appearance. This is thelargest cement found in this study. Based on its locationand morphology, this calcite cement is considered tohave been formed by meteoric diagenesis. The intergranular space of the sandstone matrix was filled with submillimeter-sized, blocky cements. No sign of hydrothermal activity was found around the brachiopod samplingsite (Minehama) or within the surrounding region.

CL images represent color information for each dot as a
mixture of R (red), G (green), and B (blue), each represented in 256 gradations from 0 to 255. The MCLI was
defined as the mean R values of a CL image. The R
values were measured using ImageJ software developed
at the National Institutes of Health, USA (ver. 1.59 m9
with Java 1.8.0_101).
After making the thin sections for CL observations,the shells were cut transversely (perpendicular to the
maximum growth axis; Fig. 3) along a transect located ~13–35 mm from the posterior shell edge. The cut surface
was etched with 0.2 mol/L hydrochloric acid (HCl) for
30 s and then coated with carbon. The surface was thenobserved using a Keyence VE-8800 SEM at the Instituteof Geology and Paleontology, Graduate School of Science, Tohoku University (IGPS), with an accelerating
voltage of 10 kV. The secondary shell layer of brachiopods is composed of calcite fibers that extend along the
maximum growth axis. During diagenesis, these calcite
fibers are dissolved and replaced with blocky calcite. The
altered fibers become amalgamated, and their outlines
become indistinct (Samtleben et al. 2001; Yamamoto etal. 2017). Traditionally, longitudinal sections are used to
examine shell microstructure (e.g., Bates and Brand
1991; Qing and Veizer 1994; Azmy et al. 1998; Korte etal. 2005), but this diagenetic alteration of fibers can beobserved more clearly in transverse sections, which enables a better determination to be made of whether or
not the fibers retained their initial forms (e.g., Samtleben
et al. 2001; Garbelli et al. 2014; Takizawa et al. 2017; Yamamoto et al. 2017).
Chemical microanalyses were performed using an Oxford Instruments energy dispersive spectrometer (EDS) installed in a JEOL JSM-7001F field emission SEM (FESEM) at the IGPS. The constant accelerating voltage for
the EDS analysis was 15 kV and the probe current 1.47 A.
We compared the microstructures of the modern andfossil brachiopod shells and defined two divisions ofpreservation state: well-preserved (Fig. 4e, f ) and diagenetically altered (Fig. 4g, h). In the well-preserved shell
portions, the outlines of the calcite fibers were well defined, and each fiber was plainly discernible. In the altered portions, the individual fibers were unobservableowing to their amalgamation. We used two indices toquantify the preservation state of shell microstructure:
altered fiber ratio (AFR) and altered fiber and punctafilling cement ratio (AF-PCR). The former is defined asa ratio (%) of the area of altered fibers to the total areaof fibers observed in a particular area (200 μm × 250 μm(magnification = × 400) or 212 μm × 266 μm (magnification = × 600)). The AF-PCR, which corresponds to the
AFR of Yamamoto et al. (2017), represents a ratio (%) of
the area occupied by altered fibers plus puncta-filling cement to the total area of the fibers where we measured

Fujioka et al. Progress in Earth and Planetary Science

SEM, energy dispersive spectrometer (EDS), and CL
observations

After the shells had been micro-sampled for isotopic
and minor element analyses, they were cut parallel tothe maximum growth axis and made into thin sections(Fig. 3). The spatial offset between the geochemical sampling and the CL sections were less than 0.5 mm. CL images of the thin sections were examined using a Relion
Industries Reliotron VII cold cathodoluminescencemicroscope mounted on a polarizing microscope at the
Department of Earth Sciences, Environmental and Resources Engineering, Waseda University, Japan. The
beam current was ~ 0.06–0.2 mA, and the voltage was
10–13 kV. The beam diameters were ~ 7 mm for the observation of modern shells and ~ 1.5 cm for the fossil
shells. We measured the mean CL intensity (MCLI) in
the corresponding areas (~ 400 μm × 1000 μm and200 μm × 2000 μm in thick and thin shell portions, respectively) of the isotopic and minor element sampling
locations to quantify the degree of luminescence. The

Fujioka et al. Progress in Earth and Planetary Sciencea(2019) 6:45

Page 7 of 23

for interval 1, as the isotopic compositions for this interval cannot be used for paleoenvironmental analysis, as
discussed below.

b

Isotopic analysis
500 µm

50 µm

c

d

20 µm

e

500 µmf

50 µm

500 µm

h

g

50 µm

500 µmiStable carbon and oxygen isotope analyses of carbonate
powder samples were performed using a Thermo Fisher
Delta V Advantage isotope ratio mass spectrometercoupled to a ThermoQuest Kiel-III automated carbonate
device, at the IGPS. The samples (~ 0.1 mg) were reactedwith 100% phosphoric acid at ~ 72 °C. The isotope ratios
were expressed in conventional (δ‰) notation and calibrated to the NBS-19 international standard relative tothe Vienna Pee Dee Belemnite (VPDB). The external
precision (1σ) based on replicate measurements (n = 91)
of the laboratory reference material (JCt-1; Okai et al.
2004) was 0.02‰ for the carbon isotope analysis and0.05‰ for oxygen isotope analysis.
It is known that the δ18O values for magnesian calcite(Mg-calcite) are higher than those for pure calcite
formed under the same conditions (e.g., Tarutani et al.
1969). However, if a fractionation correction for Mgcalcite relative to pure calcite (0.06‰ per mol% MgCO3,
according to Tarutani et al. 1969, 0.17‰ per mol%
MgCO3, according to Jiménez-López et al. 2004) is applied to δ18O values of the studied shells, this effect isnegligible or limited due to their low Mg contents (<1.18 mol% MgCO3). Therefore, the Mg effect on theδ18O values of brachiopod shells (Brand et al. 2013) does
not need to be accounted for in this study.

Minor element analysis
1 µm

Fig. 4 SEM and CL images of shell microstructure observed in thestudied brachiopod shells. a SEM image of modern Terebratalia coreanica(OTTCo). b CL image of modern T. coreanica (OTTCo)*. c SEM image ofmodern Laqueus rubellus shell (SGLR). d CL image of modern L. rubellus
shell (SGLR). e SEM image of well-preserved shell microstructure of fossil
T. coreanica (MNTCo3). f CL image in the shell portion adjacent to e, withluminescent punctae. g SEM image of altered shell microstructure(surrounded by dotted lines) in a fossil L. rubellus (MNLR2) shell. h CL
image of the shell portion adjacent to g, showing bright luminescence. i
SEM image of cement precipitated in the inter-fiber spaces of fossil T.
coreanica (MNTCo1). Image brightness and contrast were adjusted with
Adobe Photoshop software (Adobe Systems Incorporated, San Jose,
USA) so that the luminescent bands become clearly visible

the AFR. We used the two indices because the impact ofpuncta-filling cement on the diagenetic modification of
the isotopic compositions and minor element concentrations of the fossil shells is not negligible and needs to beproperly evaluated. We did not measure these indices

Powdered brachiopod shell samples (20.5–189.8 μg) weredissolved in ~ 5.0–10.0 mL of volume-specific 2% (v/v) nitric acid (HNO3). The volume of the acid was varied toadjust the Ca concentration in the solutions to ~ 3–4 ppm
for most analyses. Concentrations of the three minor elements (Mn, Fe, and Sr) were analyzed using an Agilent
7700x inductively coupled plasma mass spectrometer at
the Department of Earth and Environmental Sciences, Nagoya University, Japan. Minor elemental concentrations
are expressed as ppm (= μg/g). The precision of the analytical method, expressed as the relative standard deviation(σ) of repeated analyses of the laboratory reference material (JCt-1; Okai et al. 2004), was 1.8–4.6% for Mn, 10.8–
11.9% for Fe, and 2.2–2.4% for Sr.

Results
All analytical data are given in Additional file 1: Table
S1, Additional file 2: Table S2, Additional file 3: Table
S3, and Additional file 4: Table S4.

Fujioka et al. Progress in Earth and Planetary Science(2019) 6:45

SEM, EDS, and CL observations
Modern shells

The shells of modern T. coreanica (OTTCo) and L. rubellus (SGLR) consisted of two calcite layers: the thinnerouter primary shell layer and a thicker inner secondary
shell layer (Fig. 4a, c). The primary shell layers of bothbrachiopod species displayed a fine granular structure
measuring up to 30 μm thick in T. coreanica and up to
25 μm in L. rubellus. The secondary shell layer accounted
for > 90% of the shell thickness and was composed of thinelongated calcite fibers oriented parallel or slightly obliqueto the maximum shell growth axis. The two shell layers
were penetrated with punctae perpendicular to the outerand inner shell surfaces. The calcite fibers within the secondary shell layer were clearly identifiable. We regarded
this state as the initial fiber structure (Fig. 4a, c).
The modern shells of the two species exhibited intrinsic blue luminescence (Fig. 4b, d; Additional file 5: Figure S1-1b; Additional file 6: Figure S2–1b,) caused by alack of Mn-activated visible luminescence and by crystal
imperfections (Sippel and Glover 1965; Machel et al.
1991; Habermann et al. 1998). Here, we term this blue
luminescence as “non-luminescence.”
Fossil shells

The primary shell layer, which is commonly lost in fossil
shells (Angiolini et al. 2007; Garbelli et al. 2014, 2017),
was preserved in all fossil specimens (MNTCo1–
MNTCo5 and MNLR1–MNLR5). The secondary shelllayer of the fossil brachiopods consisted of calcite fibers(Fig. 4e) similar to those of the modern shells. However,traces of the dissolution and amalgamation of calcite fibers (Fig. 4g) were identified in many shell portions. The
punctae (< 10 μm in diameter), perforations penetratingbrachiopod shells, were scattered, commonly infilledwith calcite cements. The abundance of altered structures was highly variable among the shell portions, with
AFR values ranging from 0 to 92% and AF-PCR values
from 1 to 95%.
Some parts of the fossil shells exhibited bright luminescence in CL images (Fig. 4f, h), with MCLI values
ranging from 18 to 213 in T. coreanica and from 12 to
216 in L. rubellus. The strongly luminescent shell portions were also diagenetically altered, as indicated by thetraces of dissolution and amalgamation of calcite fibers
observed via SEM and the high AFR and AF-PCR values.
The fossil shells had luminescent dots and lines (<15 μm in diameter), each corresponding to a calcite cement filling a puncta (Fig. 5).
Submicron-sized, subhedral, blocky, isopachous fringing
calcite cements were found in the inter-fiber spaces ofsome fossil brachiopod shells with SEM (Fig. 4i). These
cements formed in a narrow space between the calcite fibers. The remnants of organic sheaths surrounding rarely

Page 8 of 23

occurred. EDS analysis indicated that the Mn concentrations of these cements were as high as 22,000 ppm andtheir Fe concentrations up to 11,000 ppm, although theconcentrations were highly variable. In contrast, Sr was
not detected in such cements.
Isotopic composition
Modern shells

The δ13C values of samples from the inner shell surfacesof modern T. coreanica from Otsuchi Bay (OTTCo)
ranged from − 0.15 to 1.38‰ and from − 0.12 to 1.75‰
for δ18O (Table 1, Fig. 6a, and Additional file 5: FigureS1-1). Interval 1 exhibited wider ranges of isotopic
values than did intervals 2 and 3, containing two local
δ13C minima and four local δ18O minima (Fig. 6a, andAdditional file 5: Figure S1-1). The δ13C profile in thisinterval consisted of lower values near the posterior shelledge and higher values near the VMR, which were separated by a local minimum δ13C value between the two
sections. The δ13C values in the lower-value section varied within a narrow range of 0.16 to 0.51‰. In contrast,
the δ13C values in the higher-value section exhibitedlarge-amplitude fluctuations within a range of − 0.15 to1.38‰. The δ18O profile exhibited large-amplitude fluctuations throughout interval 1. The δ13C and δ18O profiles in intervals 2 and 3 showed small-amplitude
fluctuations with values from 0.65 to 1.36‰ for the δ13C
values and from 0.93 to 1.75‰ for the δ18O values. Although the δ18O values in intervals 1–3 were within therange of equilibrium calcite, the δ13C values were not(Additional file 5: Figure S1-1).
The δ13C and δ18O values of samples from modern L.
rubellus from Sagami Bay (SGLR) covaried (r = 0.57, n =27, p < 0.01), ranging from 0.52 to 1.96‰ and from 0.26
to 0.94‰, respectively (Table 1, Fig. 6b, and Additional file 6: Figure S2-1). The δ13C profile showed agradual increase from 0.52 to 1.57‰ toward the VMR ininterval 1, followed by a plateau ranging from 1.49 to
1.94‰ with an average value of 1.68‰ in interval 2 anda range of 1.28 to 1.96‰ (average 1.56‰) in interval 3(Fig. 6b). The δ18O values varied within a narrow range
from 0.26 to 0.94‰ (average 0.62‰) throughout intervals 1–3. The δ18O profile showed a gradually increasing
trend in interval 1 and a decreasing trend in interval 3.
The δ13C values in interval 1 were lower than those of
equilibrium calcite, and the δ13C values in intervals 2
and 3 were slightly lower than or identical to the lowest
values of equilibrium calcite (Additional file 6: FigureS2-1). The δ18O values fell mostly in the upper half ofthe δ18O range of equilibrium calcite.
Fossil shells

The δ13C and δ18O values of the five fossil T. coreanica (MNTCo1–MNTCo5) shells fell in wide ranges

Fujioka et al. Progress in Earth and Planetary Science(2019) 6:45

Page 9 of 23

L. rubellus

T. coreanica

a

b

pn
pn

500 µm500 µmFig. 5 CL images of puncta-filling cements. CL images of the vertical sections through the studied brachiopod shells (a Terebratalia coreanica,
MNTCo2; b Laqueus rubellus, MNLR2). Note that strongly luminescent dots and lines each corresponding to a calcite cement filling a puncta

from − 3.31 to 2.43‰ for δ13C and from − 0.42 to
2.18‰ for δ18O (Table 1, Fig. 6a, and Additional file 5:
Figures S1-2–6). The δ13C profiles from interval 1 of
the fossil shells had a wider range (2.41–4.37‰) thanthat of the modern shell (1.53‰). These δ13C profiles
for interval 1 generally followed the pattern of alower-value section near the posterior shell edge anda higher-value section near the VMR. These two sections were separated by a local minimum δ13C value,with an overall increasing trend toward the VMR.
This was the same pattern seen in the modern shell.
However, the higher-value section near the VMR ofinterval 1 from two shells (MNTCo2 and MNTCo5;
Additional file 5: Figure S1-3, 6) was associated witha local minimum in δ13C values. The δ13C profiles
from intervals 2 and 3 of the fossil shells exhibited adifferent trend from the same intervals of the modern
shell. Shells MNTCo1 and MNTCo2 both showed ahigh-value plateau extending over interval 2. The
δ13C profile of MNTCo3 was similar to those of
MNTCo1 and MNTCo2 but exhibited a local minimum in this interval (Additional file 5: Figures S1-2–
4). Interval 2 of shells MNTCo4 and MNTCo5 exhibited a short high-value plateau near the VMR,
followed by a marked decrease toward the anteriorshell edge. The δ13C values in interval 3 were lower
than those of the high-value plateau in interval 2.
Shell MNTCo1 had a local δ13C minimum in thisinterval, and shell MNTCo3 had two local minima(Additional file 5: Figures S1-2, 4).
δ18O profiles of intervals 1 and 2 of the fossil T. coreanica were similar to those of the modern shell. Interval
1 had larger δ18O amplitudes than did intervals 2 and 3
as a result of a series of erratic, negative δ18O spikes.
The δ18O values were more consistent in interval 2 thanin intervals 1 and 3. Each profile from interval 2 fell in anarrow range (0.07–1.22‰), and the total range of theδ18O values from the five shells was only 1.44‰. The
δ18O values in interval 3 of the three fossil shells(MNTCo2, MNTCo4, and MNTCo5) fell in a narrow
range (0.28–0.57‰), as did the modern shell (0.82‰).
The other two fossil shells (MNTCo1 and MNTCo3) exhibited distinct negative spikes in the δ18O profiles ininterval 3 (one in MNTCo1 and two in MNTCo3; Additional file 5: Figure S1-2, 4).
The δ13C values of samples from fossil L. rubellus
shells (MNLR1–MNLR5) ranged from − 3.58 to 2.42‰,
and δ18O ranged from 0.03 to 2.37‰ (Table 1, Fig. 6b,
and Additional file 6: Figures S2-2–6). The δ13C values
in interval 1 were highly variable, and each profile had awider range (3.07–5.47‰, average 3.71‰) comparedwith the modern shell (1.05‰, Fig. 6b). The gradually
increasing trend in δ13C toward the VMR in this interval
was recognized in the fossil shells, but it was not as obvious as in the modern shell. The δ13C profiles showed
three trends in interval 2: relatively constant (MNLR1and MNLR3), increasing toward the anterior (MNLR4),
and decreasing toward the anterior (MNLR2 andMNLR5). The δ13C values were again highly variable ininterval 3 without any common trend among the fossil
shells, and almost all values were lower than those of themodern shell except for one (MNLR1).
The δ18O values of fossil L. rubellus shells were lessvaried than the δ13C values throughout the three intervals. Each profile exhibited a narrow range (1.23–
1.81‰), and the total range of the δ18O values from thefive shells was < 2.34‰.
Calcite cement

The δ13C and δ18O values of the calcite cement sample
were much lower than those of the fossil shells. The
mean values from eight repeated measurements were −17.87‰ (σ = 0.12‰) for δ13C and − 6.62‰ (σ = 0.09‰)
for δ18O (Fig. 7).

Fujioka et al. Progress in Earth and Planetary Science(2019) 6:45

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Table 1 Modern and fossil Terebratalia coreanica and Laqueus rubellus δ13C and δ18O values and minor-element concentrations
Interval 1
Sample No.

Interval 2Interval 3

Range

Average

MedianRange

Average

MedianRange

Average

MedianOTTCo− 0.15 to
1.38

0.56

0.45

1.01 to 1.36

1.19

1.19

0.65 to 1.17

1.03

1.05

MNTCo1−2.02 to 1.69

−0.43

−0.46

2.10 to 2.40

2.19

2.13

−2.98 to 1.70

0.31

0.84

MNTCo2−2.30 to 1.30

−0.64

− 0.93

1.17 to 2.15

1.81

1.96

0.06 to 0.65

0.34

0.28

MNTCo3−2.78 to 1.59

−0.05

− 0.070.59 to 1.98

1.57

1.73

−3.31 to 0.46

−1.16

−0.94

MNTCo4−1.76 to 0.65

− 0.25− 0.25− 0.03 to 2.43

1.21

1.01

−0.10 to 0.54

0.22

0.22

MNTCo5−1.89 to 2.08

0.16

0.00

−0.01 to 2.14

1.23

1.22

0.27 to 1.19

0.77

0.82

OTTCo

−0.12 to 1.75

1.04

1.12

1.17 to 1.43

1.36

1.41

0.93 to 1.75

1.39

1.47

MNTCo1−0.42 to 2.18

1.18

1.35

2.06 to 2.13

2.08

2.07

−0.21 to 2.00

1.34

1.76

MNTCo20.51 to 1.42

1.00

1.07

0.98 to 1.48

1.29

1.35

0.97 to 1.54

1.20

1.18

MNTCo30.50 to 1.62

1.11

1.22

0.93 to 1.64

1.37

1.35

0.10 to 1.36

0.70

0.75

MNTCo4−0.26 to 1.60

0.70

0.60

0.69 to 1.91

1.55

1.63

1.06 to 1.53

1.31

1.32

MNTCo50.41 to 1.83

1.33

1.38

0.99 to 1.97

1.57

1.67

1.33 to 1.61

1.51

1.55

T. coreanica
δ13C (‰ VPDB)

δ18O (‰ VPDB)

Mn (ppm)
OTTCo

2 to 105

4

3 to 74

3

2 to 85

5

MNTCo180 to 2000

480

240

90 to 260

160

130

380 to 3000

1200

1100

MNTCo2270 to 1900

770

700

390 to 3300

1100

420

580 to 2300

1600

1700

MNTCo3170 to 1800

450

240

290 to 1300

530

390

1600 to 2500

1900

1700

MNTCo4150 to 440

250

250

180 to 1700

700

570

790 to 1400

1100

1100

MNTCo5150 to 1000

450

400

230 to 2700

910

770

600 to 1600

1000

890

OTTCo

30 to 1100

250

110

50 to 800

250

70

50 to 360

15070

MNTCo1590 to 5800

1800

1200

1200 to 1900

1500

1300

2000 to 6900

3900

2900

MNTCo2200 to 2000

680

530

240 to 2400

870

400

860 to 3600

1800

1500

MNTCo3200 to 4400

1300

770

220 to 970

470

400

1200 to 3200

2000

1500

MNTCo4310 to 1500

670

580

870 to 3300

2000

1900

3800 to 4200

4000

4000

MNTCo5

1400 to 4900

2600

2100

1100 to 4700

2300

2000

2200 to 4200

3200

3400

OTTCo

810 to 1100

980

960

880 to 1000

960

960

890 to 1000

970

980

MNTCo1820 to 1000

910

920

860 to 950

910

920

810 to 960

910

910

MNTCo2730 to 950

850

850

840 to 940

890

890

850 to 920

890

880

MNTCo3790 to 1000

900

910

820 to 920

870

870

810 to 870

830

830

MNTCo4890 to 1100

980

970

780 to 990

880

870

830 to 940

890

890

MNTCo5790 to 1000

890

880

820 to 910

860

860

850 to 880

860

860

SGLR

0.52 to 1.57

1.06

1.09

1.49 to 1.94

1.68

1.68

1.28 to 1.96

1.56

1.59

MNLR1

−0.97 to 2.12

0.80

1.07

1.89 to 2.39

2.07

1.93

–

–

–

MNLR2

−1.41 to 1.74

0.21

0.33

−0.26 to 1.86

1.02

1.46

−1.51 to 0.57

−0.52

−0.41

MNLR3

−3.58 to 1.89

−0.57

−0.32

1.94 to 2.42

2.21

2.27

0.45 to 1.23

0.73

0.64

Fe (ppm)

Sr (ppm)

L. rubellus
δ13C (‰ VPDB)

MNLR4−2.65 to 0.42

−1.32

−1.50

−0.23 to 1.87

0.85

0.84

−2.82 to 0.58

−1.24

−1.49

MNLR5

−1.69 to 2.06

0.69

0.33

−1.15 to 2.23

1.10

1.60

−1.87 to 1.07

−0.21

0.18

Fujioka et al. Progress in Earth and Planetary Science(2019) 6:45

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Table 1 Modern and fossil Terebratalia coreanica and Laqueus rubellus δ13C and δ18O values and minor-element concentrations(Continued)
Interval 1
Sample No.

Interval 2Interval 3

Range

Average

MedianRange

Average

MedianRange

Average

MedianSGLR

0.26 to 0.94

0.60

0.61

0.55 to 0.93

0.74

0.73

0.26 to 0.81

0.53

0.43

MNLR1

1.14 to 2.09

1.67

1.71

2.09 to 2.33

2.19

2.17

–

–

–

MNLR2

0.74 to 1.79

1.16

1.16

0.91 to 1.96

1.53

1.73

0.24 to 1.44

0.73

0.66

MNLR3

0.03 to 1.50

0.88

1.04

1.54 to 1.85

1.69

1.68

0.96 to 1.57

1.15

0.98

MNLR4

0.29 to 1.31

0.83

0.86

1.19 to 2.00

1.59

1.55

0.53 to 1.66

1.01

0.83

MNLR5

0.63 to 1.92

1.34

1.42

0.56 to 2.12

1.61

2.00

0.31 to 1.44

0.95

1.10

10

δ O (‰ VPDB)
18

Mn (ppm)
SGLR

4 to 2097

6 to 108

7

10 to 30

20

MNLR1

150 to 760

370

310

260 to 500

380

370

–

–

–

MNLR2

170 to 1100

620

650

180 to 1200

610

530

450 to 2000

1300

1300

MNLR3

130 to 2700

1100

680

170 to 260

210

200

800 to 2100

1300

1200

MNLR4

490 to 1900

1100

930

260 to 700

380

280

410 to 1700

1200

1300

MNLR5

160 to 940

410

340

120 to 1900

710

240

760 to 1000

900

920

SGLR

70 to 10,100

1300

620

70 to 1200

310

120

100 to 3600

1100

510

MNLR1

410 to 3900

1000

640

1200 to 3200

2000

1600

–

–

–

MNLR2

180 to 5000

1100

400

230 to 750

500

500

1300 to 5800

3200

2800

MNLR3

340 to 2700

1200

1200

440 to 4900

1900

510

2000 to 4200

2800

2600

MNLR4

600 to 1500

1100

1000

400 to 940

640

610

900 to 3400

2500

2900

MNLR5

510 to 3100

1300

1000

830 to 4700

2000

1600

2700 to 5100

3500

3200

SGLR

860 to 1100

990

1000

800 to 860

830

820

870 to 980

920

930

MNLR1

930 to 1000

980

970

880 to 920

900

900

–

–

–

MNLR2

850 to 1000

920

930

830 to 890

860

850

820 to 970

890

880

MNLR3

730 to 1000

870

890

850 to 860

850

850

810 to 1000

890

890

MNLR4

800 to 880

840

830

830 to 870

850

850

730 to 940

820

800

MNLR5

870 to 970

920

920

800 to 890

840

830

900 to 1000

950

950

Fe (ppm)

Sr (ppm)

Minor elements
Modern shells

The minor element concentrations (n = 30) in the modern T. coreanica shell fell within the ranges of 2–10 ppm(mean = 5 ppm, σ = 3 ppm, median = 4 ppm) for Mn, 30–
1100 ppm (mean = 220 ppm, σ = 260 ppm, median = 100ppm) for Fe, and 810–1100 ppm (mean = 980 ppm, σ =80 ppm, median = 980 ppm) for Sr (Table 1, Fig. 6a, andAdditional file 5: Figure S1-1). The profiles of these elements showed no systematic variations.
In the modern L. rubellus shell, minor element
concentrations (n = 27) ranged from 4 to 30 ppm(mean = 10 ppm, σ = 6 ppm, median = 8 ppm) for Mn,
70 to 10,100 ppm (mean = 1000 ppm, σ = 2000 ppm,
median = 510 ppm) for Fe, and 800–1100 ppm(mean = 940 ppm, σ = 90 ppm, median = 920 ppm) for Sr(Table 1, Fig. 6b, and Additional file 6: Figure S2-1) andalso showed no systematic variations.

Fossil shells

The minor element concentrations (n = 127) in thefossil T. coreanica (MNTCo1–MNTCo5) shells varied
between 80 and 3300 ppm (mean = 580–1100 ppm,
σ = 470–800 ppm, median = 280–740 ppm) for Mn, 200
and 6900 ppm (mean = 1000–2600 ppm, σ = 930–1700
ppm, median = 600–2200 ppm) for Fe, and 730 and1100 ppm (mean = 870–930 ppm, σ = 50–80 ppm, median = 860–920 ppm) for Sr (Table 1, Fig. 6a, andAdditional file 5: Figures S1-2–6).
In the fossil L. rubellus shells, minor element concentrations (n = 103) of (MNLR1–MNLR5) fell in the ranges ofFujioka et al. Progress in Earth and Planetary Sciencea(2019) 6:45

bPage 12 of 23

posterior shell edge toward the VMR and increased toward the anterior shell edge. In contrast, the Sr concentrations in the fossil shells (T. coreanica, 730–1100 ppm;
L. rubellus, 730–1000 ppm) were comparable with thoseof the modern shells (T. coreanica, 810–1100 ppm; L.
rubellus, 800–1100 ppm). As with the modern shells, nodiscernable patterns were seen in the Sr profiles.
Calcite cement

The minor element concentrations of the calcite cement
sample were 6200 ppm for Mn, 14,400 ppm for Fe, and440 ppm for Sr. Mn concentration was 6 times higher thanthe median concentrations of the fossil shells, and the Feconcentration was 7 times higher. The Sr concentration of
the cement was lower than that of the fossil shells.

Discussion
The diagenetic modification of isotope compositions

Fig. 6 Profiles of geochemical, microstructural, and optical signals inthe studied brachiopod. These panels compare the δ13C and δ18O
values, minor element concentrations, mean CL intensity (MCLI),
altered fiber ratio (AFR), and altered fiber and puncta-filling cement
ratio (AF-PCR) between the modern (OTTCo and SGLR) and fossil(MNTCo1–MNTCo5 and MNLR1–MNLR5) shells. a Terebratalia
coreanica shells. b Laqueus rubellus shells. The geochemical profilesof each sample were fitted to the average length of interval 2 (7.74mm for T. coreanica and 5.27 mm for L. rubellus)

120–2700 ppm (mean = 400–1000 ppm, σ = 200–830 ppm,
median = 370–910 ppm) for Mn, 180–5800 ppm (mean =1300–1900 ppm, σ = 830–1800 ppm, median = 670–1500ppm) for Fe, and 730–1000 ppm (mean = 840–960 ppm,
σ = 40–70 ppm, median = 830–970 ppm) for Sr (Table 1,
Fig. 6b, and Additional file 6: Figures S2-2–6).
Roughly speaking, the Mn and Fe concentrations in
the fossil shells of both species decreased from theThe δ13C and δ18O profiles in interval 1 of the modern
T. coreanica shell are characterized by the occurrence of
two local δ13C minima and four local δ18O minima.
Similar depletions are found in the same interval of themodern L. rubellus shell, although they are not so distinct as those in the T. coreanica shell. Interval 1 includes the region of the shell to which the diductor andadjustor muscles are attached (Shiino and Kitazawa
2010) and a shell cavity where the digestive and reproductive organs are housed (Williams and Rowell 1965).
This suggests that the observed δ18O minima are potentially related to the biological activities of the brachiopods, although we cannot specify the exact mechanism.
The δ13C values of the muscle scar are up to 2‰ lower
than those of the secondary shell layer (Parkinson et al.
2005; Yamamoto et al. 2010a, 2013) due to secondary
calcification, which has been reported in the muscle
scars, loop, and teeth (Williams 1968). Therefore, it ishighly likely that the depletion of the δ13C values ininterval 1 is caused by precipitation and/or dissolution(Hughes et al. 1988) around the specialized portions.
The δ13C amplitude in intervals 2 and 3 of the fossil
brachiopods is ~ 7.0–7.5 times greater than those ofmodern shells, and the δ18O amplitude is ~ 3 times
greater. The δ13C and δ18O values of these intervals inthree T. coreanica and four L. rubellus shells display significant positive correlations (T. coreanica: r = 0.89–0.98,
p < 0.01, excluding MNTCo2 and MNTCo4; L. rubellus:
r = 0.88–0.99, p < 0.01, excluding MNLR1) (Fig. 7). Both
δ13C and δ18O trend negatively toward the δ13C andδ18O values of the calcite cement. The δ18O value of calcite precipitated in oxygen isotope equilibrium with meteoric water in northeastern Japan, including the
Minehama region (δ18O of meteoric water = − 7.7 to −10‰ VSMOW; Mizota and Kusakabe 1994) at the mean

Fujioka et al. Progress in Earth and Planetary Science(2019) 6:45

Page 13 of 23

Fig. 7 Cross-plots of δ13C versus δ18O values of the studied brachiopod shells. The samples were extracted from the modern and fossil T.
coreanica and L. rubellus shells. The cement δ13C versus δ18O values are also plottedannual temperature (11.2 °C, Japan Meteorological
Agency 2018) is estimated to be − 6.62 to − 8.92‰ following Friedman and O’Neil (1977). The δ18O of the calcite cement (− 6.62‰) falls within this range, indicatingthat the δ13C and δ18O values of the highest endmembers on the cross-plots are close to their initialvalues and that the isotopic values of brachiopod shells
at Minehama decreased toward those of the cement during meteoric diagenesis.
Another explanation for the positive correlation of theδ13C and δ18O values is a kinetic isotopic fractionation
effect. Kinetic isotope fractionation during CO2 hydration and hydroxylation results in an enhanced incorporation of 12C and 16O during precipitation of skeletal
carbonates (McConnaughey 1989a, 1989b; McConnaughey et al. 1997; Auclair et al. 2003; Yamamoto et al.
2013; Takayanagi et al. 2015). This effect is closely related to rapid growth rates and high metabolic activity
and is typically characterized by a positive correlation
between δ13C and δ18O values (or δ13C–δ13CEC andδ18O–δ18OEC values). However, it is reported thatgrowth rates along the inner surface (i.e., shell thickening rates) of brachiopod shells, including T. coreanica
and L. rubellus, are very slow and that within a single

shell, the kinetic effect is negligible there (Yamamoto etal. 2010b, 2013). The δ13C and δ18O values of interval 1
are less strongly correlated than those of intervals 2 and
3 (Fig. 7). This is because the isotopic composition ininterval 1 of the fossil shells is influenced by the biogenic
effect mentioned above as well as by meteoric diagenetic
modification.
The isotopic data indicate that the highest endmembers on the cross-plots (Fig. 7) are likely to be closest
to the initial shell δ13C and δ18O values. The highest endmembers are from samples extracted from the thick portion of interval 2. This portion corresponds to “interval 2”of Pleistocene K. hanzawai shells from the Ryukyu Islands(Takizawa et al. 2017), which was regarded as a good shell
portion to use for paleoenvironmental reconstructions because it exhibited relatively small intra-shell and intraspecies variations. Therefore, this interval is likely to be agood region of the shells for paleoenvironmental analysis
in many brachiopod taxa.
The diagenetic modification of minor element
concentrations

Minor element concentrations in carbonate minerals
have been used to identify diagenetically altered(2019) 6:45

Page 14 of 23

brachiopod shells or shell portions (e.g., Wenzel 2000;
Ullmann et al. 2014). As meteoric water generally contains more Mn and Fe and less Sr compared with seawater, Fe and Mn concentrations increase and Srconcentration decreases in diagenetically altered marine
carbonates (Brand and Veizer 1980; Marshall 1992).
The Mn concentrations in the studied modern shells are
relatively uniform. Concentrations in T. coreanica fallwithin a narrow range of 2–12 ppm, and L. rubellus concentrations are between 4 and 30 ppm (Fig. 6a, b). These
ranges are comparable with values reported in previous
studies of modern brachiopod shells (5–500 ppm, Morrison and Brand 1986; 0–200 ppm, Brand et al. 2003; 4–30
ppm, Lee et al. 2004; 0–70 ppm, Ullmann et al. 2017) andare lower than the common Mn concentrations in modern shells (< 80 ppm) compiled by Brand et al. (2003).
In contrast, the Mn concentration in the fossil T. coreanica and L. rubellus shells is higher than that of the modern shells. The observed range is 80–3300 ppm in the T.
coreanica shells and is 120–2700 ppm in the L. rubellus
shells. These values exceed the common Mn concentration in modern shells (Brand et al. 2003) and indicate that
there are significant intra-shell and intra-species variationsin the fossil brachiopod Mn concentrations (Fig. 6). The
samples with high Mn concentrations did not correspondto specific regions of the shells but exhibited low δ13C andδ18O values, high Fe concentrations, and strong luminescence (Fig. 6, Additional file 5: Figures S1-2–6, and Additional file 6: Figures S2-2–6). This indicates that theincreased Mn concentrations are the result of meteoric
diagenetic alteration.
Although some anomalously high Fe concentrations (>600 ppm) are observed, the range of Fe concentrations in
the modern T. coreanica shells ranged from 30 and 490
ppm and from 70 to 570 ppm in L. rubellus (Fig. 6a, b).
These values exceed the common Fe concentrations ofmodern brachiopod shells (< 140 ppm) presented by
Brand et al. (2003). This difference is at least partly due tothe fact that the Fe concentration threshold reported in
Brand et al. (2003) was derived from bulk shell samples,
which represent spatially averaged values.
The Fe concentrations in the fossil T. coreanica (200 to
6900 ppm) and L. rubellus (180 to 5800 ppm) shells aremuch higher than those of the modern shells and thecommon Fe concentration range (Brand et al. 2003). The
samples with high Fe concentrations also exhibited highMn concentrations, low δ13C and δ18O values, and strong
luminescence. As with Mn, anomalously high Fe concentrations also occur in the fossil shells. These anomalously
high concentrations are not always associated with any
microstructural (dissolution and amalgamation of fibers),
optical (strong luminescence on CL images; see below), or
geochemical (decreased δ13C or δ18O values or increased
Mn concentration) signals of diagenetic alteration. As

such, we consider that these anomalously high Fe concentrations are likely not diagenetic products but represent
initial concentrations from when the brachiopods werealive. Similar anomalously high Fe concentrations without
signs of diagenetic alteration in well-preserved fossil (~ 20
and ~ 70 ka) K. hanzawai shells have also been describedby Takizawa et al. (2017).
Unlike Mn and Fe concentrations, Sr concentrations in
the modern and fossil brachiopod shells were similar andtheir ranges overlap (Table 1). This indicates that Sr concentration in these brachiopod shells is not likely to be agood indicator of diagenetic alteration. The Mn and Srconcentrations show a moderate negative correlation (fossil T. coreanica: r = − 0.46, p < 0.01, Fig. 8c; fossil L. rubellus: r = − 0.52, p < 0.01, Fig. 8d). This differs from theresult of Jelby et al. (2014), who found that Mn/Ca of diagenetically altered Lower Maastrichtian brachiopod shells
was strongly negatively correlated with Sr/Ca (r = − 0.94).
The Mn concentrations in the calcite cement were ~2–3 times higher than the maximum Mn concentrationsin the fossil shells, and Fe concentrations were ~ 2 times
higher. This indicates that Mn and Fe concentrations inbrachiopod shells at Minehama increased during meteoric diagenesis, approaching those of the cement. The
Sr concentrations in the calcite cements were ~ 50% orless of mean Sr concentrations in the fossil shells. Thisimplies that Sr concentrations in brachiopod shells at
Minehama decreased during meteoric diagenesis, approaching those of the cement. However, the decrease in
the Sr concentrations was relatively more gradualthan the increase in the Mn and Fe concentrations.
This is the reason why Sr is not sensitive to diagenesis at Minehama and shows a moderate negative correlation with the Mn concentrations. In conclusion,
our study shows that of the three minor elements analyzed in this study, Mn concentration is the most reliable indicator of diagenetically altered shells or shell
portions.

Fujioka et al. Progress in Earth and Planetary Science

Diagenetic alteration detected by CL image observations

Cathodoluminescence observations are useful for determining the paragenetic sequences of diagenetic products
precipitated from the solutions containing Mn. Alteredshell portions are easily detectable by luminescence activated by the presence of Mn. It has been shown that theδ13C and δ18O values of luminescent shell portions arecommonly lower than those of non-luminescent portions (e.g., Grossman et al. 1993; Mii et al. 2012).
The modern T. coreanica and L. rubellus shells exhibit
faint to weak luminescent bands that are arranged almost parallel to the inner shell surface (Fig. 4b, d; Additional file 5: Figure S1-1b, and Additional file 6: Figure
S2-1b). Similar luminescent bands are observed in shellsof modern inarticulate brachiopods and in those of otherFujioka et al. Progress in Earth and Planetary Science(2019) 6:45

Page 15 of 23

a

b

c

d

e

f

Fig. 8 Cross-plots of minor element (Mn, Fe, and Sr) concentrations in the studied brachiopod shells. The samples were extracted from themodern and fossil T. coreanica (a, c, e) and L. rubellus (b, d, f) shells

marine invertebrates (Barbin and Gaspard 1995; Barbin
2013; Riechelmann et al. 2016). These bands or lines are
the result of biological activity (e.g., bleeding cycles andchanges in growth rates) and/or environmental stresses(e.g., input of coastal water, tidal rhythms, and changes
in seawater temperature). In the present study, it is difficult to determine the main reason for the difference in
the CL intensity between the modern shells of the two
species, noting that CL can also be influenced by themeasurement conditions (England et al. 2006).

The fossil shells display brighter luminescence thanthat of the modern shells. No luminescent bands are observed in the fossil shells. The MCLI profiles of the fossil
brachiopod shells show statistically significant positive
correlations with Mn concentration (T. coreanica: r = 0.73,
n = 122, p < 0.01; L. rubellus: r = 0.51, n = 103, p < 0.01)(Figs. 6a, b and 9a–c). The luminescent regions also correspond to the samples with higher Fe concentrations andlower δ13C and δ18O values than those of adjacent nonluminescent regions within an individual shell (Fig. 6a, b),

Fujioka et al. Progress in Earth and Planetary ScienceaMean CL intensity

255(2019) 6:45

although no such material was observed in the studied
modern shells, and void spaces are created during postmortem decomposition, with subsequent precipitation ofdiagenetic cements (Garbelli et al. 2016). We conclude
that the presence of carbonate cements with extremely
high Mn and Fe concentrations in the punctae andinter-fiber spaces is one of the major causes of high concentrations of these elements in diagenetically alteredshell portions, as discussed below.

T. coreanica
Interval 1
Interval 2Interval 3100

MNTCo1
MNTCo2
MNTCo3
MNTCo4
MNTCo5The diagenetic alteration of shell microstructurer = 0.73, p < 0.01, n = 122

10
10

255

Mean CL intensity

100

1000

10000

Mn (ppm)b100

L. rubellusInterval 1
Interval 2Interval 3
MNLR1
MNLR2
MNLR3
MNLR4
MNLR5

r = 0.51, p < 0.01, n = 103

10
10

100

1000

10000

Mn (ppm)c
255

Mean CL intensity

Page 16 of 23100
MNTCo1–5
MNLR1–5

r = 0.64, p < 0.01, n = 225

10
10

100

1000

10000

Mn (ppm)
Fig. 9 Double-logarithmic cross-plots of mean CL intensity versus
Mn concentration in the studied fossil shells. a T. coreanica. b L.
rubellus. c Combined data from both species

indicating that these shell portions have been altered bymeteoric diagenesis.
The punctae of the fossil brachiopods are partly to
fully filled with cement and display bright luminescence(Fig. 4f, h) as has been described in other species (e.g.,
Takizawa et al. 2017; Casella et al. 2018). This is because
the punctae are filled with organic material in live brachiopods (Williams 1997; Pérez-Huerta et al. 2009),

The secondary shell layer is composed of calcite fibers,
each with a concave outer surface and convex inner surface (Gaspard 1991; Samtleben et al. 2001). However, altered fibers become irregularly shaped and amalgamatedwith an increased diagenetic alteration. The amalgamation of two or more fibers occurs locally in modern
brachiopods, but the outline of such fibers remains defined, which means that pristine amalgamated fibers canbe distinguished from diagenetically altered fibers (Samtleben et al. 2001).
Altered shell portions (Additional file 5: Figures S1-2–
6 and Additional file 6: Figures S2-2–6) are characterized by low δ13C and δ18O values, high Mn and Fe concentrations, and luminescent CL images. In contrast, thewell-preserved shell portions exhibit comparatively high
δ13C and δ18O values, low Mn and Fe concentrations,and weakly luminescent or non-luminescent CL images(Fig. 4f ). AFR and AF-PCR are correlated negatively with
δ13C and δ18O but positively with Mn and Fe concentrations and MCLI in the fossil T. coreanica and L. rubellus
shells (Fig. 10).
Some studies have argued that the impact of in-fillingcements in punctae upon the chemical and isotopic
composition of shells is negligible because their volume
accounts for only a small portion of the shell (e.g., < 10%of a Silurian brachiopod, Resseralla elegantula, shells;
Samtleben et al. 2001) compared with that of the shellforming calcite fibers. However, if the isotopic compositions and chemical concentrations of the puncta-fillingcements are one or more orders of magnitude greaterthan those of the shell-forming fibers, the impact of suchcements on the geochemistry of spot samples might not
be negligible. Here, we assume that the isotopic composition and Mn and Fe concentrations of the puncta-fillingcements are identical to those of the cement formed bymeteoric diagenesis (δ13C = − 18‰, δ18O = − 7‰, Mn
concentration = 6000 ppm, Fe concentration = 14,000ppm). The δ13C values are at least 19‰ lower than thoseof the fossil shells, and the δ8O values are 9‰ lower.
The Mn concentrations are at least 5000 ppm higher
than those of the fossil shells, and Fe concentrations are
12,000 ppm higher. Under this assumption, if the punctae of the studied modern shells are filled with such

Fujioka et al. Progress in Earth and Planetary Science(2019) 6:45

Page 17 of 23

a

b

c

d

e

f

g

h

Fig. 10 Cross-plots of isotopic composition versus AFR or AF-PCR (a, b, e, and f) and of isotopic composition versus MCLI (c, d, g, and h) . The
gray bar on the y-axis indicates a range of δ13C or δ18O values of the modern brachiopod shell (OTTCo or SGLR)

cements and they account for 5% of the shell volumes,
then the δ13C and δ18O values decrease by ~ 1‰ and ~0.4‰, respectively (Table 2). Conversely, the Mn and Fe
concentrations increase by ~ 300 and ~ 600 ppm,

respectively. In fact, the punctae account for 1–9% of
the fossil T. coreanica shell volumes and 1–12% of the L.
rubellus shell volumes. These indicate that the isotopic
composition and chemical concentration of the puncta-

Fujioka et al. Progress in Earth and Planetary Science(2019) 6:45

Page 18 of 23

Table 2 Effect of puncta-filling cements to the isotopic composition and minor element concentrations of shell samples. We
assume that the isotopic composition and minor element concentrations of the puncta-filling cements are identical to those of thecement formed by meteoric diagenesis. Then, we calculate the isotopic composition and minor element concentrations of the
mixtures of shell and puncta-filling cements when the punctae are filled with such cements
Modernshell

Cement Puncta filling cements accounting for 5% of the shell Puncta filling cements accounting for 10% of the shell
volumesvolumes
Shell + cement

Δ*

Shell + cementΔ*

1.01 to 1.36 − 18

0.06 to 0.39

− 0.96− 0.89 to − 0.58

− 1.92

δ18O (‰) 1.17 to 1.43 − 7

0.76 to 1.01

− 0.420.35 to 0.59

− 0.83

T. coreanica
Interval 2
δ13C (‰)

Mn (ppm) 3**

6000

310

300

610

600

Fe (ppm)

70**

14,000

770

700

1500

1400

Sr (ppm)

960**

400

930

− 30

900

− 60

1.49 to 1.94 − 18

0.52 to 0.94

− 0.99− 0.46 to 0.05

− 1.97

δ O (‰) 0.55 to 0.93 − 7

0.17 to 0.53

− 0.39− 0.21 to 0.14

− 0.78Mn (ppm) 7**

6000

300

300

600

590

Fe (ppm)

120**

14,000

810

690

1500

1380

Sr (ppm)

820**

400

800

− 20

780

− 40

L. rubellusInterval 2
δ13C (‰)
18*Δ = “shell + cement” − “modern shell”**Median

filling cements can potentially significantly bias the isotopic composition and minor element concentrations ofspot or bulk shell samples.
AF-PCR was correlated more negatively with δ13C
and δ18O and more positively with Mn and Fe concentrations and MCLI than was AFR (Table 3, Fig. 9).
This suggests that the occurrence of puncta-filling cements is one of the major causes of diagenetic modification of isotopic compositions and minor element
concentrations. However, it is not clear whether thepuncta-filling cements have similar isotopic compositions and minor element concentrations to cements
formed by meteoric diagenesis. The punctae of somemodern brachiopod shells are luminescent (e.g.,
Griesshaber et al. 2007; Barbin 2013), indicating thatthey are filled with carbonate minerals that areenriched in Mn compared with shell calcite. It is deduced that such puncta-filling cements are chemical
and/or microbial precipitates formed in a closed reductive space (e.g., Kaźmierczak and Iryu 1999) orbiogenic products. As such, the puncta-filling cementsin this study might include carbonate minerals of different origins, with likely differences in their isotopic
composition and minor element concentrations.
Figure 10 shows the cross-plots of isotopic composition
versus AFR/AF-PCR and isotopic composition versus
MCLI. The intercepts of these cross-plots can be regarded
as the isotopic composition of non-altered brachiopod

shells (AFR or AF-PCR = 0, MCLI = 0), theoretically corresponding to the initial isotopic composition of the fossil
brachiopod shells. The intercepts are not identical but areclose to each other (the difference in δ13C values is <1.1‰ and in δ18O values is < 0.6‰). The intercepts of theδ18O values of the fossil T. coreanica shells are up to
0.5‰ greater than the δ18O values of the modern shellfrom Otsuchi Bay. Those of L. rubellus are 2‰ greaterthan the δ18O values from Sagami Bay. Assuming that thebrachiopods occupied similar habitats during the Pliocene
to those occupied by their modern counterparts, this indicates the presence of cooler and/or more saline seawaterin the Minehama region during the Pliocene comparedwith that of the modern Otsuchi and Sagami bays. This
interpretation is supported by the occurrence of coolwater molluscan species within the outcrop from which
the fossil brachiopod shells of this study were collected(MH1; Amano et al. 2011). This suggests that AFR/AFPCR and MCLI are good indices for quantitatively estimating the extent of diagenetic alteration within brachiopod shells.
The submicron-sized cements in a narrow space in
the inter-fiber spaces (Fig. 4i) show the morphologicaland geochemical features that are common in cements formed during meteoric diagenesis (Tucker andWright 1990), and the occurrence of such cements is
an additional cause of high concentrations of Mn and
Fe in diagenetically altered shells.

Fujioka et al. Progress in Earth and Planetary Science(2019) 6:45

Page 19 of 23

Table 3 Cross-correlations between geochemical, microstructural and optical signals in the studied fossil brachiopodCrosscorrelations are calculated between isotope composition (δ13C and δ18O), minor-element (Mn, Fe, and Mn) concentrations, MCLI,
and AFR or ΑF-PCR of the fossil Terebratalia coreanica and Laqueus rubellus shells. Coefficient values in brackets are not statisticallysignificant (p > 0.01)
δ13C (‰VPDB)

δ18O (‰
VPDB)

Mn
(ppm)

Fe
(ppm)

Sr
(ppm)

Mean CL intensity(MCLI: 0–255)

Altered fiber and puncta-fillingcement ratio (AF-PCR: %)Fossil T. coreanica and L. rubellus (n = 36)
δ13C (‰VPDB)

1

δ18O (‰VPDB)

0.9

1

Mn (ppm)

−0.71

−0.71

1

Fe (ppm)

−0.51

−0.43

0.61

1

Sr (ppm)[0.21][0.18][−0.42] [−0.02] 1

Mean CL intensity (MCLI: 0–255)

−0.53

−0.54

0.77

[0.34][−0.23] 1

Altered fiber and puncta-fillingcement ratio (AF-PCR: %)

−0.75

−0.76

0.75

0.6

[−0.15] 0.61

1

Fossil T. coreanica (n = 22)
δ13C (‰VPDB)

1δ O (‰VPDB)

0.9

1

Mn (ppm)

−0.77

−0.72

Fe (ppm)[−0.48][− 0.35]

0.54

1

Sr (ppm)

0.54

0.55

−0.68

[− 0.19] 1

18

1

Mean CL intensity (MCLI: 0–255)

−0.65

−0.64

0.80

[0.20]−0.47

Altered fiber and puncta-fillingcement ratio (AF-PCR: %)

−0.79

−0.81

0.77

0.62

[−0.44] 0.63

1
1

Fossil L. rubellus (n = 14)
δ13C (‰VPDB)

1δ O (‰VPDB)

0.91

1

Mn (ppm)[−0.65]− 0.72

1

Fe (ppm)[−0.57][− 0.56]

0.76

Sr (ppm)[−0.15][− 0.20][− 0.16] [0.17]

18

1
1

Mean CL intensity (MCLI: 0–255)[−0.32][−0.37]0.69[0.62][0.05]

1

Altered fiber and puncta-fillingcement ratio (AF-PCR: %)−0.71− 0.710.71[0.57][0.31][0.55]

The cross-correlation coefficients of isotopic composition, minor element concentration, and MCLI and AFPCR indices indicating the alteration of shell portions
are presented in Table 3. The δ13C and δ18O values ofthe fossil T. coreanica and L. rubellus shells show moderate to strong negative correlations with Mn concentration, MCLI, and AF-PCR. Mn concentration, MCLI, and
AF-PCR were positively correlated. The negative correlation of Fe concentration with isotopic composition is
weaker than that of Mn concentration because of the occurrence of localized high Fe concentrations that are
more anomalous than the high Mn concentrations. Fe
concentration shows a weak (although not statisticallysignificant (p > 0.01)) positive correlation with MCLI.
Mn and Fe concentrations increase with increased diagenetic alteration and act as an activator (Mn) and aquencher (Fe) for CL images (Machel et al. 1991). The

1

weak positive correlation of Fe concentration with MCLI
indicates that the activator (Mn) acts more efficiently as
an activator than Fe does as a quencher. Sr concentration was not correlated significantly with any other features or measures. In summary, shell portions with highMn concentration, high MCLI, and high AF-PCR generally exhibit low δ13C and δ18O values, indicating thatthese measures are useful for detecting shell portions altered by meteoric diagenesis.
Lithologic control on the diagenetic alteration ofbrachiopod shells

Our study shows that the four indices commonly used to
specify diagenetically altered carbonates—δ13C and δ18O
values, minor element concentrations, the preservation
state of shell microstructure, and cathodoluminescence—
are applicable to brachiopod shells. However, it is known

(2019) 6:45

Page 20 of 23

that diagenesis alters the initial paleoenvironmental signals
extracted by these indices (Ullmann and Korte 2015). Yamamoto et al. (2017) studied the four indices of fossilized
Kikaithyris hanzawai shells from the Pleistocene reef complex deposits (Iryu et al. 2006) and showed that although altered fibers are commonly observed in brachiopod shells,
the initial isotopic composition can be largely preserved,
and luminescent shells cannot always be regarded as having
undergone degradation of shell microstructure or isotopic
modification by diagenesis. The findings of those authors
indicate that CL images are not always sufficient for detecting diagenetic alteration in shells. This is at least partly because of the differences in the diagenetic processes
modifying the chemical and isotopic compositions between
brachiopod shells embedded in siliciclastic and volcaniclastic deposits and those in carbonate deposits. The geochemistry of brachiopod shells embedded in siliciclastic andvolcaniclastic deposits is affected by formation water relatively rich in Mn, which originates from meteoric water.
This can explain why diagenetically altered shells are luminescent in CL images, have low δ13C and δ18O values, andhigh Mn concentrations. In contrast, carbonate deposits
have limited sources of Mn, except when the deposits areassociated with siliciclastics (including paleosols) or volcaniclastics. As such, CL images might not necessarily be useful for the detection of diagenetic alteration of shells incarbonate deposits.
The relationship between the degree of preservationof shell microstructures and the initial isotopic composition has been controversial. It is known that some
Paleozoic brachiopods, in spite of their well-preserved
shell microstructure, have low δ13C and δ18O values,
similar to those of diagenetically altered marine carbonate fossils and sparry cements (Rush and Chafetz
1990), or exhibit large variations in isotopic composition caused by a diagenetic alteration (Banner andKaufman 1994). To explain this conflict, it has beensuggested that only large-scale dissolution and subsequent recrystallization of shells can result in isotopic
resetting in the per mil range (Wadleigh and Veizer
1992; Qing and Veizer 1994). However, the significantly lower δ13C and δ18O values in intervals 2 and
3 of the fossil brachiopod shells compared with thoseof the modern shells in the present study indicatethat the resetting of isotopic values in the per mil
range can occur without large-scale dissolution andsubsequent recrystallization.
Shell portions in which microstructures are preserved
but their initial isotopic composition has been modified
present a significant challenge with respect to reconstructing paleoceanographic conditions. Applying and crosschecking multiple criteria to assess diagenetic alteration
are required to distinguish between diagenetically alteredand unaltered brachiopod shells (Yamamoto et al. 2017).

Conclusions
To estimate the extent of modification in the isotope
composition of fossil brachiopod shells with increasing
diagenetic alteration, we analyzed δ13C and δ18O andthree commonly applied indicators of meteoric diagenesis: minor element (Mn, Fe, and Sr) concentrations,cathodoluminescence, and shell microstructure. The
samples for these analyses were collected from the innersurfaces of fossil T. coreanica and L. rubellus (rhynchonellate brachiopod) shells collected from conglomeratesof the Tentokuji Formation (Pliocene, 3.85–2.75 Ma) exposed in northeastern Japan. The results of the study
can be summarized as follows:

Fujioka et al. Progress in Earth and Planetary Science(1) Individual shells of T. coreanica and L. rubellus canbe divided into three intervals (intervals 1–3) basedon the shell morphology, each with characteristic
chemical and isotopic compositions.
(2) Interval 2 is characterized by relatively small intrashell and intra-species variations in δ13C and δ18O
values in both modern and fossil shells. The δ13C
and δ18O values from this interval of the fossil
shells plots as the highest end-member, and thesevalues are therefore likely to be the closest to theinitial shell δ13C and δ18O values.
(3) Of the three minor elements examined in thisstudy, Mn concentration is the most reliableindicator of diagenetically altered shells. Mn and Fe
concentrations in the fossil brachiopod shells arehigher than those of the modern shells, displaying
large intra-shell and intra-species variations, withseveral anomalously high localized concentrations.
The samples with high Mn and Fe concentrations
do not correspond to specific regions of the shells
but also exhibit low δ13C and δ18O values andstrong luminescence. This indicates that the increased Mn concentrations are the result of meteoric diagenetic alteration. The anomalously highFe concentrations, which are also observed in modern shells, are not necessarily associated withmicrostructural (dissolution and amalgamation of fibers), optical (strong luminescence on CL images),or isotopic (decreased δ13C or δ18O values). This
indicates that these anomalously high Fe concentrations are likely not diagenetic products but represent initial concentrations from when thebrachiopods were alive. Unlike Mn and Fe concentrations, Sr concentrations in the studied modern
and fossil brachiopod shells are similar and theirranges overlap, indicating that Sr concentration incarbonate minerals is not always a good indicator
for identifying diagenetic alteration.
(4) We quantified the preservation state of shell
microstructure using two indices: altered fiber ratio(2019) 6:45

Page 21 of 23(AFR) and altered fiber and puncta-filling cement
ratio (AF-PCR). To quantify the degree of luminescence, we measured the mean cathodoluminescenceindex (MCLI) defined as the mean R value in a particular area of a CL image. The δ13C and δ18O
values of the fossil brachiopod shells are moderately
or strongly negatively correlated with Mn concentration, MCLI, and AF-PCR. Mn concentration,
MCLI, and AFR/AF-PCR are positively correlatedwith each other. Fe concentration shows a weaker
negative correlation with isotopic composition thandoes Mn concentration on account of the occurrence of anomalously high localized Feconcentrations.

Authors’ contributions
FH, HT, and YI conceptualized and designed this study. FH and YI conducted
the fieldwork and sampling. FH, HT, and KY carried out the chemical andisotope analyses. HT and YI collaborated with FH in the interpretation of thedata and the construction of the manuscript. All authors read and approved
the final manuscript.

Our study provides further evidence that applying andcross-checking multiple criteria to assess diagenetic alteration is the optimal method for distinguishing between
diagenetically altered and unaltered brachiopod shells.

Author details
1
Department of Earth Science, Graduate School of Science, Tohoku
University, Sendai 980-8578, Japan. 2Department of Earth and Environmental
Sciences, Nagoya University, Nagoya 464-8601, Japan.

Fujioka et al. Progress in Earth and Planetary Science

Funding
This work was financially supported by the Japan Society for the Promotionof Science KAKENHI (Grant-in-Aid for Scientific Research) Grant numbers
2134052 and 26302008 to YI.
Availability of data and materials
Please contact the corresponding author regarding data requests.
Competing interests
The authors declare that they have no competing interests.

Received: 28 December 2018 Accepted: 16 May 2019

Additional files
Additional file 1: Table S1. δ13C and δ18Ο values of the modern
Terebratalia coreanica (OTTCo) and Laqueus rubellus (SGLR) shells. (XLSX 13 kb)
Additional file 2: Table S2. δ13C and δ18Ο value, AFRs (altered fiber
ratios), and AF-PCRs (altered fiber and puncta-filling cement ratios) of thefossil Terebratalia coreanica (MNTCo1–MNTCo5) and Laqueus rubellus(MNLR1–MNLR5) shells. (XLSX 26 kb)
Additional file 3: Table S3. Minor element (Mn, Fe, and Sr)concentrations of the modern Terebratalia coreanica (OTTCo) and Laqueus
rubellus (SGLR) shells. (XLSX 13 kb)
Additional file 4: Table S4. Minor element (Mn, Fe, and Sr)concentrations and MCLIs (mean CL intensities) of the fossil Terebratalia
coreanica (MNTCo1–MNTCo5) and Laqueus rubellus (MNLR1–MNLR5) shells.
(XLSX 23 kb)
Additional file 5: Figure S1. Sampling spots, δ13C and δ18O values,
minor element (Mn, Fe, and Sr) concentrations, mean CL intensities, alteredfiber ratios, and altered fiber and puncta-filling cement ratios of the modern(Figure S1-1, OTTCo) and fossil (Figures S1-2–6, MNTCo1–MNTCo5) T. coreanica shells. Composite CL images are presented for each shell. SEM and CL
images of selected shell portions are also shown. Red and blue arrows indicate local minima in δ13C and δ18Ο, respectively. (ZIP 26310 kb)
Additional file 6: Figure S2. Sampling spots, δ13C and δ18O values, minor
element (Mn, Fe, and Sr) concentrations, mean CL intensities, altered fiber
ratios, and altered fiber and puncta-filling cement ratios of the modern (Figure
S2-1, SGLR) and fossil (Figures S2-2–6, MNLR1–MNLR5) L. rubellus shells. Composite CL images are presented for each shell. SEM and CL images of selected
shell portions are also shown. (ZIP 25125 kb)
Additional file 7: Doc. S1. Estimation of δ13C and δ18O values of
equilibrium calcite. (DOCX 25 kb)

Abbreviations
AF-PCR: Altered fiber and puncta-filling cement ratio; AFR: Altered fiber ratio;
CL: Cathodoluminescence; MCLI: Mean CL intensity

Acknowledgements
We are grateful to T. Sato for providing the information on the geologic settingof Minehama. The manuscript was significantly improved by the comments
and suggestions of K. Ikehara (editor) and two anonymous reviewers.

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