Materials and setting

R/V Yayoi, based at the International Coastal Research Center, Atmosphere and Ocean Research Institute (ICRS/AORI), The University of Tokyo, collected living T. crossei and T. coreanica on 12 September 2005 from the mouth of Otsuchi Bay (70 m water depth; 39°21.86′N, 141°59.97′E) on the Sanriku Ria Coast in northeastern Honshu, Japan (Figure 1). The bay is semienclosed, characterized by a narrow mouth (∼3 km from north to south), and extends ∼8 km from east to west. Detailed data on seawater temperature and salinity at the brachiopod growth site, adjacent stations (Oki-no-shima Station, Station B, and Station 8), and two stations close to Otsuchi Bay (Todogasaki Station and Ozaki Station) were provided by Yamamoto et al. (2011). Bottom-water samples were collected at the brachiopod growth site using a 6 L Vandorn water sampler on 12 September 2005, 12 December 2005, 22 March 2006, 5 June 2006, 27 July 2006, and 30 October 2006.

High-resolution and three-dimensional sampling

Following the method of Yamamoto et al. (2010a, b), we collected the four series of samples for isotopic analyses from the secondary shell layer of ventral valves (Yamamoto et al., 2011) as below. Terms for the series follow Auclair et al. (2003) and Yamamoto et al. (2010a. b).

1) Ontogenetic series: This series of samples was taken from the outermost part (outer surface) of the secondary shell layer, along an “ontogenetic” transect corresponding to the growth axis of the shell (TCr-Ont, T. crossei; TCo-Ont, T. coreanica) (Figure 1B and 1D), to investigate fluctuations in δ13C and δ18O values reflecting seasonal and annual variations in temperature and/or isotopic compositions of ambient seawater. The sampling intervals for TCr-Ont and TCo-Ont are 0.13–0.33 mm and 0.11–0.25 mm, respectively.

2) Isochronous series: This series of samples was collected from the outermost part (outer surface) of the secondary layer (Figure 1B and 1D). The sampling points for T. crossei (TCr-Iso) and T. coreanica (TCo-Iso) range from 4 to 37 mm and from 4 to 25.5 mm from the growth axis of the shell, along a growth line, at intervals of 2–4 mm and 2–3 mm, respectively. The samples in this series are considered to have been precipitated simultaneously under the same environmental conditions, which enabled us to decipher potential kinetic and metabolic effects on the isotopic compositions at various growth rates.

3) Depth series: This series of samples was taken at different depths below (= at different distances from) the outer surface of the secondary shell layer (Figure 1B and 1D). Samples were collected at depths ranging from 0.3– 0.9 mm at depth intervals of 0.15–0.25 mm for T. crossei (TCr-D1 and TCr-D2) and from 0.3–2.55 mm at depth intervals of 0.2–0.25 mm for T. coreanica (TCo-D1, TCo-D2, and TCo-D3). Each sample was collected at the particular depth in a groove ∼5 mm long and 0.15–0.2 mm wide that was cut in the outer surface of the secondary shell layer. The grooves were parallel to the growth axis of the shell. These samples were used to assess the potential evolution of isotopic compositions of the secondary shell layer during shell thickening.

4) Inner series: This series of samples was taken from the innermost part of the shells (inner surface of the secondary shell layer) at intervals of 3 mm for T. crossei (TCr-In) and 2 mm for T. coreanica (TCo-In) along a line parallel to (TCr-In) or slightly oblique to (TCo-In) the ontogenetic transect (Figure 1C and 1E).

Samples for the ontogenetic, isochronous, and inner series were collected within <0.1 mm depth from the outer and inner surfaces of the secondary shell layer.

Carbon- and oxygen-isotope analyses

Stable-isotope analysis of carbonate material (∼0.1 mg) was performed using a Finnigan MAT 252 mass spectrometer coupled with a Kiel-III automated carbonate device at Technological Research Center of Japan Oil, Gas and Metals Corporation (JOGMEC). δ¹³C and δ18O values of powdered carbonate samples were calibrated to the NBS-19 international standard relative to Vienna Pee Dee belemnite (VPDB). External precision (1σ) for δ13C and δ18O analyses, based on replicate measurements, was ±0.02‰ and ±0.03‰, respectively. Following the methods of Sampei et al. (2005) and Yamamoto et al. (2010a), δ13C_DIC of seawater was analyzed using a Finnigan Delta Plus mass spectrometer at Graduate School of Environmental Studies, Nagoya University. Additionally, δ13C_DIC of seawater was measured following a simple headspace method, combined with a gas chromatograph/combustion furnace/isotoperatio mass spectrometer (Miyajima et al., 1995), at AORI. We used the average values for δ13C_DIC (δ, VPDB) determined at the two institutions. External precision (1σ) for δ13CDIC analyses, based on replicate measurements, was ±0.2‰. We evaluated correlations of δ13C and δ18O values of brachiopod shells using the reduced major axis regression technique (Sokal and Rohlf, 1994), the significance of which was examined statistically using the two-sided Pearson test, with a 99% confidence limit.

Figure 1.

A, topography of Otsuchi Bay (Yamamoto et al., 2011). Solid circles indicate the brachiopod growth site and the stations where oceanographic data were recovered. B–E, photographs of the ventral valves of T. crossei and T. coreanica showing the lines along which samples for isotopic analyses were collected; B, outer surface of the ventral valve of T. crossei showing the ontogenetic series TCr-Ont, the isochronous series TCr-Iso, and the depth series TCr-D1 and TCr-D2; C, inner surface of the ventral valve of T. crossei showing the inner series TCr-In; D, outer surface of the ventral valve of T. coreanica showing the ontogenetic series TCo-Ont, the isochronous series TCo-Iso, and the depth series TCo-D1, TCo-D2, and TCo-D3; E, inner surface of the ventral valve of T. coreanica showing the inner series TCo-In.

Isotopic compositions of equilibrium calcite

Seawater δ¹³C_DIC values at the brachiopod growth site off Otsuchi Bay ranged from 0.4 to 1.2‰ (Table 1). These values are consistent with previously reported δ¹³C_DIC values (0.6–1.2‰) for surface water (0–500 m water depth) at a site off Japan (34°25′N, 142°00′E) (Kroopnick, 1985). Because the concentration of dissolved phosphorus in seawater is closely related to the photosynthesis-respiration cycle (Broecker and Peng, 1982), the relative effects of biological processes on δ13CDIC can be assessed with respect to variations in PO_43- using the relationship defined by Broecker and Maier-Reimer (1992), which describes the change in δ13C_DIC resulting from the photosynthesis-respiration cycle as a function of the change in PO₄3- (Δδ13C_DIC = 1.1 × ΔPO_43- where PO_43- is in μmol/kg). ICRS/AORI measured seasonal variations in concentrations of dissolved PO₄3- in seawater at Station 8 in Otsuchi Bay from October 1999 to May 2000. The values range from 0.24 to 0.70 μmol/L, indicating that the biologically influenced seasonal variation in δ13C_DIC would be ∼0.5‰. Taking into account analytical errors and difference in timing of water-sample collections, this is roughly consistent with the measured variation (∼0.8‰) in seawater δ13C_DIC values at the brachiopod growth site. Following the method of Yamamoto et al. (2010a, b), we calculate the δ13C values of equilibrium calcite at the study site to be 1.4 to 2.6‰.

In our previous article (Yamamoto et al., 2011), δ18O values of equilibrium calcite were estimated using seawater δ¹⁸O (δ¹⁸O_water) values ranging from -0.38 to 0.08‰ (Table 1) and their excellent linear relationship with salinity (δ¹⁸O_water = 0.66 × salinity - 22.41; r = 0.98). The δ18O values of equilibrium calcite at the brachiopod growth site range from -1.4 to 2.4‰ for the years 1990–2005.

Table 1.

Data for seawater samples collected from the brachiopod growth site.

Carbon- and oxygen-isotope compositions of brachiopod shells Terebratulina crossei

The δ13C values of TCr-Ont samples range from -3.65 to 1.78‰, whereas δ18O values range from -1.77 to 2.66‰ (Table 2); both exhibited significant seasonal variations throughout the series (Figure 2A). The amplitude of seasonal cycles decreased in the third stage, as defined by Yamamoto et al. (2011). Although the δ¹³C peaks mostly correspond with the δ18O peaks, small differences in their peak positions may exist. The major positive peaks in δ18O values represent the coldest periods during the winter (March–April) (Yamamoto et al., 2011). Each annual cycle may also contain one or two minor (<1‰) δ¹⁸O positive peaks. The δ¹³C and δ¹⁸O values display significant positive correlations (r = 0.79, n = 378), with the slope of the regression line being 1.18 (Figure 3A). The ontogenetic δ13C values are mostly less than those of equilibrium calcite. However, the TCr-Ont samples collected near the posterior and anterior shell edges may fall within the range of δ13C values of equilibrium calcite. By contrast, the δ18O values are largely identical to those of equilibrium calcite.

The δ13C and δ18O values of TCr-Iso samples correlate negatively with growth rate. Both values from low-growth-rate portions (portions far from the growth axis) are up to 1.5‰ greater than those from high-growth-rate portions (portions near the growth axis) (Figure 4A). The δ18O values of the samples from this series fall within the range of equilibrium calcite. The δ13C values are less than those of equilibrium calcite near the growth axis but increase with distance from the axis (i.e., with decreasing growth rates) to be identical to the latter. The cross-plots of δ13C versus δ18O values reveal positive correlations (r = 0.92, n = 14), with the slope of regression being 1.28 (Figure 4C).

The δ¹³C and δ¹⁸O values of the TCr-D1 and TCr-D2 samples do not vary regularly with depth in the secondary shell layer (Figure 5A–B). The δ13C values of the TCr-D1 samples decrease slightly (0.5‰) with depth, whereas the δ18O values are relatively constant. The δ13C values of the TCr-Ont samples collected immediately above the TCr-D1 samples range from -2.37 to 0.87‰, and the δ¹⁸O values range from -0.26 to 2.07‰. These δ13C and δ18O values are identical to or less than those of the TCr-D1 samples. Although the δ13C values of the TCr-D2 samples decrease with depth (by 1‰), the δ18O values increase slightly with depth (by 0.5‰). The δ13C values of the TCr-D1 and TCr-D2 samples are less than those of equilibrium calcite. By contrast, the δ18O values are identical to those of equilibrium calcite.

Table 2.

δ13C and δ18O values of T. crossei and T. coreanica. The δ18O values of the TCr-Ont and TCo-Ont samples were provided in the auxiliary material of Yamamoto et al. (2011).

Continued.

Continued.

The δ13C and δ18O values of the TCr-In samples range from 1.05 to 1.59‰ and from 1.63 to 1.93‰, respectively. The δ13C values are slightly less than or identical to those of equilibrium calcite. By contrast, all the δ18O values fall within the range of those of equilibrium calcite (Figure 5F). No regular relationships are recognized between the two variables.

Terebratalia coreanica

The δ13C values of the TCo-Ont samples vary between -6.35 and 0.57‰, whereas the δ18O values range between -2.97 and 1.61‰ (Figure 2B). The δ¹⁸O profile exhibits distinct seasonal variations from the posterior shell edge to the anterior shell edge; each major positive peak represents the coldest period during the winter (March–April) (Yamamoto et al., 2011). One or two minor (<0.8‰) δ18O positive peaks are often superimposed on each annual cycle. Although the amplitude of the δ18O cycles is roughly constant (∼3‰), the annual mean δ18O values tend to decrease toward the anterior shell edge, deviating from those of equilibrium calcite. Although the δ13C values decrease significantly from ∼0 to -5‰ at the earlier ontogenetic stage (near the posterior shell edge) and then fluctuate within an approximate range from -6 to -3.5‰, the profile does not correlate well with the δ18O profile or the time series of water temperature. The cross-plots of δ13C versus δ18O values of the TCo-Ont samples display significant positive correlations (r = 0.70, n = 215), with the slope of regression being 1.33 (Figure 3B). The δ¹³C values are exclusively less than those of equilibrium calcite.

Theo δ13C and δ18O values of the TCo-Iso samples correlate negatively with growth rates. The δ13C and δ18O values from low-growth-rate portions are up to ∼3.2 and ∼2.5‰ greater, respectively, than those from high-growth-rate portions (Figure 4B). With decreasing growth rates, the δ18O values increase and fall within the range of those of equilibrium calcite. By contrast, the δ13C values are exclusively less than those of equilibrium calcite. The δ13C and δ18O values display strong positive correlations (r = 0.98, n = 10), with the slope of regression being 1.15 (Figure 4D).

The δ¹³C and δ¹⁸O values of the TCo-D1 samples decrease by ∼1.5‰ with depth, which is followed by a slight increase of ∼0.5‰ (Figure 5C). In contrast, the isotopic values of the TCo-D2 and TCo-D3 samples do not exhibit any regular trend with depth (Figure 5D–E). The δ13C and δ18O values of the samples from all depth series are less than and identical to those of equilibrium calcite, respectively. The δ13C and δ18O values of the TCo-Ont samples collected immediately above the TCo-D1 and TCo-D2 samples are identical to or less than those of the latter. The TCo-In samples have the δ13C values (0.83– 1.21‰) that are less than those of equilibrium calcite (Figure 5G). The δ18O values are identical to those of equilibrium calcite.

Figure 2.

Variations in δ13C and δ18O values of the TCr-Ont (A) and TCo-Ont (B) samples. Shaded areas represent ranges of estimated δ13C and δ18O values of equilibrium calcite. Dashed lines denote annual cycles in δ18O values, which are defined by their major positive peaks. Minor positive peaks of δ18O values are indicated by arrows in the graphs. Black (solid, open, and broken) arrows at the upper part of the graphs indicate the positions of major growth lines on the shell surface. Three stages (first, second, and third stages) were defined by Yamamoto et al. (2011).

Figure 3.

Cross-plots of δ13C versus δ18O values of the TCr-Ont (A) and TCo-Ont (B) samples. Values from samples from muscle scars and TCr-In and TCo-In samples are also plotted.

Figure 4.

Variations in δ13C and δ18O values of the TCr-Iso (A) and TCo-Iso (B) samples. Cross-plots of δ13C versus δ18O values of the TCr-Iso (C) and TCo-Iso (D) samples. Shaded areas represent ranges of estimated δ13C and δ18O values of equilibrium calcite. Average isotopic values of the ontogenetic series at 34.67–35.21 mm and 26.28–26.81 mm from the posterior shell edges, respectively, for T. crossei and T. coreanica are indicated.

Kinetic and metabolic effects

Kinetic processes are caused by kinetic isotope fractionation during CO₂ hydration and hydroxylation, resulting in a depletion of 13C and 18O in precipitating skeletal carbonates (McConnaughey, 1989a, b; McConnaughey et al., 1997; Auclair et al., 2003). This effect is closely related to a fast growth rate and a high metabolic activity and is typically characterized by a positive correlation between δ13C and δ18O values. Therefore, the positive correlation of δ13C versus δ18O values of the ontogenetic- and isochronous-series samples for T. crossei and T. coreanica (Figures 3A–B, 4C–D) can be ascribed to the kinetic isotope fractionation effect. However, the correlative relationships between the δ13C and δ18O values are different between the two species, sug gesting species dependency of the kinetic effect. The kinetic effect is apparent in δ13C and δ18O values of the isochronous samples. Although the isochronous samples were secreted under the same environmental conditions, the TCr-Iso and TCo-Iso samples do not have uniform isotopic compositions (Figure 4A–B) and show increases in the δ13C and δ18O values from the high-growth-rate portions (portions near the growth axis) toward the low-growth-rate portions (portions far from the growth axis) (Figure 4C–D). These results contrast well with those of Lee and Wan (2000), who reported no kinetic effect on δ13C and δ¹⁸O of fossil brachiopod shells.

Figure 5.

Variations in δ13C and δ18O values of the depth-series (A–E) and inner-series (F, G) samples. Ranges of δ13C and δ18O values of the ontogenetic-series samples collected immediately above TCr-D1, TCo-D1, and TCo-D2 are shown. Shaded areas represent ranges of estimated δ13C and δ18O values of equilibrium calcite.

Figure 6.

Cross-plots of δ13C versus δ18O values of the TCr-Ont samples in the first, second, and third stages (A) and TCo-Ont samples in the first and second stages (B). The periods for the stages are shown in Figure 2.

Skeletal carbonates, such as corals, show depletion in 13C compared with equilibrium calcite, which can be explained, in part, by a metabolic effect (McConnaughey, 1989a; McConnaughey et al., 1997; Rollion-Bard et al., 2003). This effect is clearly recognized on cross-plots of δ13C versus δ18O values as a difference in the δ13C values between equilibrium calcite and the higher δ13C- and δ18O-value end members. Such a difference is clearly discernible on the cross-plots of δ13C versus δ18O values of the ontogenetic- and isochronous-series samples of T. coreanica, but it is not recognized in T. crossei (Figure 3). This evidence indicates that the degree of the metabolic effect differs depending on species.

The cross-plots of δ13C versus δ18O values of the TCr-Ont and TCo-Ont samples yield different regression slopes ranging from 0.57 to 1.56 depending on growth stages (Figure 6). The regression line of δ13C versus δ18O for the third stage of the TCr-Ont series shows a much more gentle slope (0.57) compared with those established for the other stages of the TCr-Ont (1.15– 1.56) and TCo-Ont (1.06–1.23) samples. The third stage of the TCr-Ont series is characterized by very slow growth rates. Therefore, metabolic activity is low during this stage, which results in a minor incorporation of respiration-derived 12C and in the precipitation of 13C-enriched shell calcite. This process is responsible for the gentle slope of the regression line compared with other stages.

The δ18O and δ13C values of the TCr-In samples are plotted with the higher δ13C- and δ18O-value end members (Figure 3A). In contrast, those of the TCo-In samples have greater δ13C values than the end members (Figure 3B). This indicates that the inner samples are affected least by the kinetic effect and that the degree of the metabolic effect is different between the two species. The marginal mantle of brachiopods is involved in secretion at the shell margin comprising the primary layer and upper part of the secondary shell layer. The observed offsets in the δ13C values from those of the equilibrium values (Figure 3) suggest that the marginal mantles of the examined brachiopods have greater metabolic activity than the posterior mantle whose cells contribute to shell thickening, and hence would incorporate more 12C-enriched carbon derived from respiration. This hypothesis agrees well with data reported by Rosenberg et al. (1988), who investigated the metabolism and shell-growth dynamics of Terebratalia transversa. They evaluated the metabolic rates of mantle tissue through its degree of consumption of 14C-labeled carbohydrates. Their results showed that the metabolic rates of mantle tissue are 3.7 times greater in the leading marginal edge than in its “posterior” portion, which is in good agreement with carbon isotope records of the brachiopod species mentioned above.

The δ13C values of the TCr-In samples are identical to and slightly lower than those of equilibrium calcite, whereas the TCo-In samples have lower δ13C values than equilibrium calcite. Again, this indicates that the degree of the metabolic effect varies greatly with species. Although the sampling interval is extensive, no significant variations are recognized in the isotopic profiles of the inner-series samples of T. crossei and T. coreanica. This indicates that metabolic and thermal variations are not recorded in the inner series regardless of species, which can be explained by isochronous accretion of the inner surface of the secondary layer during shell thickening and a time-averaging effect due to slow rates of shell thickening.

For T. crossei and T. coreanica, the depth-series samples collected immediately below the ontogenetic-series samples are identical to or, more commonly, enriched in ¹³C and ¹⁸O compared with the latter (Figure 5 A, C–D). The enrichment may imply that shell thickening occurred at slow rates. The isotopic profiles of the depth series do not display significant variations, with the exception of TCo-D1 (Figure 5), which is due to the fact that formation of the inner surface of the secondary layer is affected least by the kinetic effect, as well as a time-averaging effect due to slow rates of shell thickening.

Growth curves and growth lines

Seasonal variations in δ18O values of the ontogenetic-series samples and their comparison with those of equilibrium calcite (Yamamoto et al., 2011) enabled us to construct growth curves for these brachiopods. The growth rate of the T. crossei specimen used in this study appears to be a logarithmic curve, reaching a plateau at the age of ∼10 years; it was thought to have lived for ∼14.5 years (Figure 7). Although the T. coreanica specimen did not reach ontogenetic maturity, it lived for ∼5.5 years (Figure 7). Rapid shell growth began at ∼3–5 years in both species. The growth curves established for T. crossei and T. coreanica are similar to that of L. rubellus (Yamamoto et al., 2010a). However, they are different from those of T. transversa (Paine, 1969; Auclair et al., 2003) in that the latter has a rapid growth period at the early stage (ages of <3 years) of their lives (Figure 7).

Although brachiopods have visible growth lines on the shell surface (Figure 1B and 1D), the mechanisms of their formation are poorly understood (Hiller, 1988; Hughes et al., 1988; Rosenberg et al., 1988). In contrast, environmental factors and physiological constraints are responsible for growth line formation in bivalve-mollusk shells. Three types (types I, II, and III) of growth lines are recognized in T. crossei and T. coreanica (Figure 2A– B), as in L. rubellus (Yamamoto et al., 2010a). Types I and II growth lines are defined as those lines corresponding closely to the positive and negative peaks, respectively, of the ontogenetic δ18O profiles. All other lines are categorized as type III. Taking into account the location of the growth lines in the isotopic profile, we believe that types I and II growth lines may have formed annually in the lowest and highest seawater temperature, respectively. One type I growth line formed during a short duration of decreased seawater temperature. However, there are many positive and negative peaks in the ontogenetic profiles that do not correlate with any growth line. Type III growth lines are located between the positive and negative peaks of the ontogenetic profiles. Curry (1984) found that biannual spawning (late spring and late autumn) is common in temperate terebratulid brachiopods. At least some type III growth lines may have formed at the time of reproduction (Figure 2A–B). These confirm one of the conclusions in our previous study, namely, that growth lines of L. rubellus, which also has the three types of growth lines, do not necessarily form periodically and that their numbers cannot be used to estimate the ages of individuals (Yamamoto et al., 2010a).

Figure 7.

Growth curves for T. crossei and T. coreanica estimated from seasonal variations in δ18O values of the TCr-Ont and TCo-Ont samples, respectively. For comparison, growth curves for L. rubellus (Yamamoto et al., 2010a) and T. transversa (Paine, 1969; Auclair et al., 2003) are shown.

Evaluation of isotopic compositions as paleoenvironmental proxies

The results of this study indicate that isotopic signals of brachiopod shells must be used carefully as paleoenvironmental indicators, because the physiological effects that influence δ13C and δ18O values vary, even within a single shell. When reconstructing secular variations in ancient seawater δ13C_DIC values and temperature and/or δ18O_SW values using brachiopod shell δ13C and δ18O values, respectively, a particular portion of the shell from specimens belonging to the same taxonomic group should be used to exclude the isotopic variations that occur within a shell and among taxa. Yamamoto et al. (2011) discussed the availability of δ18O values of T. crossei and T. coreanica in detail and showed that the δ18O records of the first stage of the ontogenetic series are the most reliable environmental proxies, because they are nearly identical to equilibrium calcite. This good agreement allows an estimation of seawater temperature with a high degree of accuracy (∼1°C), using the temperature dependency of calcite δ18O values (Friedman and O'Neil, 1977).

The δ13C values of the TCr-Ont samples collected near the posterior and anterior shell edges may fall within the range of those of equilibrium calcite. The ontogenetic δ13C profiles are much less variable near the anterior shell edge than near the posterior shell edge. The average of the TCr-Ont samples collected within 5 mm and 10 mm from the anterior shell edge are ∼1.0 and 1.2‰. These are very close to the minimum δ13C value of equilibrium calcite (1.4‰). Therefore, the anterior shell edge would be suitable for a proxy of δ13C_DIC values of ancient seawater.

The δ13C values of the TCr-In and TCo-In samples are relatively constant and slightly less (0.2–0.8‰ for T. crossei and 0.6–1.0‰ for T. coreanica) than those of equilibrium calcite (Figure 5F–G). Therefore, these portions would be useful to estimate δ13C_DIC of ancient seawater. However, samples for isotopic analyses should not be collected from muscle scars of T. crossei and T. coreanica, even though they lie on the inner surface of the secondary shell layer. This portion has δ13C values that are up to ∼1.7‰ less than those of the inner series (Figure 3A–B), which may be due to the fact that muscle scars experience respiration or continual dissolution and precipitation processes (Hughes et al., 1988).

The δ18O values of the TCr-In and TCo-In samples fall within the range of equilibrium calcite (Figure 5F–G). The seawater temperatures calculated from the average δ18O values (1.8‰ for TCr-In and 1.4‰ for TCo-In) are ∼7 and 8°C, respectively. These correspond to the winter seawater temperature at the brachiopod growth site off Otsuchi Bay (Yamamoto et al., 2011).

Fossil brachiopods that are taxonomically (at species or genus level) close to T. crossei date back to the Jurassic (Williams et al., 2002). Fossil T. coreanica occurs from the Miocene onward (Williams et al., 2002). If high temporal-resolution analysis can be applied to fossils that are not fragmented and have not been diagenetically altered, we will be able to reconstruct ancient ocean environments more accurately than is possible at present. The high growth rates of the two brachiopod species allow for a high temporal-resolution-sampling technique. For the ontogenetic series, the resolution in this study is as high as ∼5 days/sample for T. crossei and ∼7 days/sample for T. coreanica, which enables the recognition of short-term environmental changes.