Lawrence Berkeley National Laboratory Recent Work

Title Nacre tablet thickness records formation temperature in modern and fossil shells

Permalink https://escholarship.org/uc/item/1rf2g647

Authors Gilbert, PUPA Bergmann, KD Myers, CE et al.

Publication Date 2017-02-15

DOI 10.1016/j.epsl.2016.11.012

Peer reviewed

eScholarship.org Powered by the California Digital Library University of California Bivalve nacre preserves a physical indicator of paleotemperature

Pupa U.P.A Gilbert1,2*, Kristin D. Bergmann3,4, Corinne E. Myers5,6, Ross T. DeVol1, Chang-Yu Sun1, A.Z. Blonsky1, Jessica Zhao2, Elizabeth A. Karan2, Erik Tamre2, Nobumichi Tamura7, Matthew A. Marcus7, Anthony J. Giuffre1, Sarah Lemer5, Gonzalo Giribet5, John M. Eiler8, Andrew H. Knoll3,5

1 University of Wisconsin–Madison, Department of Physics, Madison WI 53706 USA. 2 Harvard University, Radcliffe Institute for Advanced Study, Fellowship Program, Cambridge, MA 02138. 3 Harvard University, Department of Earth and Planetary Sciences, Cambridge, MA 02138. 4 Massachusetts Institute of Technology, Department of Earth, Atmospheric and Planetary Sciences, Cambridge, MA 02138. 5 Harvard University, Department of Organismic and Evolutionary Biology, Cambridge, MA 02138. 6 University of New Mexico, Department of Earth and Planetary Sciences, Albuquerque, NM 87131. 7 Advanced Light Source, Lawrence Berkeley National Laboratory, Berkeley, CA, 94720, USA. 8 California Institute of Technology, Division of Geological and Planetary Sciences, Pasadena, CA 91125 * [email protected], previously publishing as Gelsomina De Stasio

Abstract:

Biomineralizing organisms record chemical information as they build structure, but to date chemical and structural data have been linked in only the most rudimentary of ways. In paleoclimate studies, physical structure is commonly evaluated for evidence of alteration, constraining geochemical interpretation. Thermodynamics, however, predicts that temperature will affect both physical and chemical components of biomineralized skeletons, and thus structural and geochemical data might provide complementary or compensatory information on ancient climates. We test this hypothesis and find that patterns of nacre ultrastructure in modern and fossil shells from the bivalve family

Pinnidae correlate strongly with the thermodynamically controlled, multi-isotope based, carbonate clumped isotope thermometer. Mean nacre tablet thickness increases with clumped isotope temperature of formation, indicating that abiotic factors moderate the 1 physical process of biomineralization at the ultrastructure scale. Thus we describe a new type of paleothermometer less, and differently, susceptible to diagenesis, useful in shallow shelf environments.

Introduction:

Fossils record evolutionary dynamics in the marine realm over the past 100 million year (1, 2), and geochemical proxies document marked climatic variation through the same interval (3). The integration of these paleobiological and paleoclimatic records, however, can be challenging because the skeletal fossils that document marine animal evolution come mostly from shallow continental shelf and platform environments, while the most widely used indicators of marine paleoclimate are deposited primarily on the deep sea floor (3, 4). Oxygen isotopes have been used to infer paleotemperatures for shelf environments, but, while useful, these are subject to diagenetic alteration. To complement geochemical data and more effectively bridge the records of climate and marine animal evolution, one would like independent paleotemperature proxies from invertebrate fossils themselves. Novel, cost-effective proxies would provide not only more direct integration of global diversity, biogeographic, and climatic trends, but would also permit regional comparisons of intertwined biotic and environmental dynamics. Here we report a promising proxy that meets this need – a physical indicator of paleotemperature recorded in the nacre of bivalved mollusks from the family Pinnidae. We evaluate this proxy by comparing the physical structure of nacre in pinnid bivalves though geologic time with a geochemical proxy for temperature: carbonate clumped isotope thermometry.

2 We chose to focus on pinnid bivalves for several reasons. The Pinnidae, or pen shells, are fast growing, sessile, suspension-feeders that are widespread in tropical to subtropical, coastal and shallow shelf environments, both today and in the past (5-10). The fossil record of the Pinnidae goes back to the Carboniferous Period, with first occurrences of the genus Pinna in the Middle Mississippian (~345Ma) and the genus Atrina in the Middle

Triassic (~247Ma) (estimates based on a Paleobiology Database, PBDB, search for “Pinna” and “Atrina” on 5.25.15) (Figure S1). Their shell morphology is unique and easily identified even from (frequently encountered) fragmental remains. Like many other marine bivalves, pen shells combine an outer layer of prismatic calcite (CaCO3) and inner nacre layer. Nacre, or mother-of-pearl, is a lamellar composite of aragonite (CaCO3) tablets and organic sheets (11, 12). Uniquely, in the Pinnidae, prismatic calcite and nacreous aragonite layers easily separate as the shells dry, providing two distinct carbonate minerals to analyze using carbonate clumped isotope thermometry. When present in the fossil record, shells tend to be well preserved although the prismatic and nacre layers rarely remain attached.

In this study we quantify the physical parameters of nacre ultrastructure, including nacre tablet thickness (TT), and compare them to independent estimates of temperature based on carbonate clumped isotope analysis for both modern and ancient shells of the sister taxa Pinna and Atrina. The three modern shells sample a range of latitudes and seasonal temperatures (coastal Florida, USA; Mallorca, Spain; and Bocas del Toro, Panama).

The carbonate clumped isotope temperatures and TT can be directly compared to nearby buoy sea surface temperature measurements; they are in good agreement, increasing our confidence in clumped isotope paleotemperature estimates from fossil specimens. Seven

3 fossil specimens were analyzed, drawn from three locations reflecting geologic warm times and places (the Late Cretaceous Gulf Coastal Plain, ~ 65.5-66 Ma (13-16); the Early Eocene

Gulf Coastal Plain, ~ 52-54 Ma (17-19); and the Middle Miocene Mid-Atlantic Calvert Cliffs,

~ 12.7-13.2 Ma) (20).

Tests for Diagenetic Alteration

If nacre is to provide a reliable indication of ancient shallow water paleotemperatures, we must first demonstrate that it can be preserved intact over long time intervals. Figure 1 shows results from both PhotoElectron Emission spectromicroscopy (PEEM) for Polarization-dependent Imaging Contrast (PIC)-mapping

(21-23) and x-ray absorption spectra at the oxygen K-edge (24), for both modern and

Cretaceous shells. The modern and ancient specimens are essentially identical, documenting mineralogical and crystallographic preservation on nearly 70 million year timescales. In particular, the x-ray absorption spectra extracted from microscopic areas of aragonite and calcite are identical to those from geologic and synthetic aragonite and calcite first published by DeVol et al. (24). X-ray diffraction also demonstrates that nacre and prismatic layers are still aragonite and calcite, respectively, as shown in Figure S2.

The late Cretaceous shell Ps5 is also extremely well preserved chemically. EPMA measurements, both maps and transects, indicate that Fe and Mn trace metal concentrations are extremely low across the shell (aragonite: mean 110 ± 12 and 90 ± 10 ppm; calcite: 202 ± 42 and 93 ± 27 ppm respectively, ± std. error of the mean). As both metals tend to incorporate into calcite and aragonite in reducing environments below the sediment-water interface, this suggests minimal diagenesis (25). Sr and Mg are consistent

4 with primary precipitation of the two phases from seawater (aragonite: mean 2567 ± 71 ppm and 0.013 ± 0.003%; calcite: 986 ± 38 ppm and 0.391 ± 0.019% respectively, ± std. error of the mean). Secondary ion mass spectrometry (SIMS) δ18O analysis of six transects across Ps5 demonstrate consistent δ18O values (δ18O 1σ = 1.1‰) across the shell, which is incompatible with small-scale isotopic alteration (Figure S3).

Thus, both crystallographic and chemical analyses confirm excellent preservation and lack of diagenetic alteration of crystal structure in these and most other areas of the fossil shells. Diagenetic change was observed sporadically in the PIC-maps, predominantly near cracks, where water presumably penetrated, dissolved and re-precipitated aragonite tablets with greater than normal orientation of c-axis angle spreads, as shown in Figure S4.

Nacre Tablet Thickness in Modern and Ancient Shells

Figure 2 shows PIC-maps of shells from each of the four geologic epochs in this study: Modern, Miocene, Eocene, and Late Cretaceous. In PIC-maps, color (hue and brightness) illustrates crystal orientation in each 20nm pixel. Thus, Figure 2 shows that each aragonite tablet behaves as a single crystal and is similar, though not identical, in orientation to other tablets (within 15°). This is consistent with previous observations (26,

27). Tablet layers are interspersed with 30nm-thick organic sheets (28), visible as black lines in Figure 2A,B but not always preserved in fossils (Figure 2C,D). The orientation-color contrast, therefore, enables identification of individual tablets even where organics are absent, e.g., in the blue tablets below the word “Eocene” in Figure 1C. This permits the observation and measurement of tablet thicknesses (TT) in samples of variable preservation and age.

5 We analyzed three modern (Figures S5-S7) and seven fossil pen shells (Figures S8,

S9), with a continuous series of overlapping PIC-maps (full set in Figure S10), always in the same location in the shell, that is, the thickest nacre region magnified in Figure S6, and indicated by red arrows in Figures S5, S7, S9. For all specimens average TT was measured by dividing the vertical field of view of each image by the number of tablet layers present.

PIC-maps that did not show tablet layers horizontally were rotated prior to thickness measurements, and the number of nacre tablets layers in each PIC-map was counted digitally, as shown in Figure S11 and described in detail in the SM Methods. In Figure S12 we present the results of all TTs in each shell cross-section, which shows the variability of

TT through time as nacre is deposited. As Figure 2 illustrates, mean tablet thickness is larger for intervals known to be relatively warm (Eocene, Cretaceous) than it is for cooler intervals (Miocene and modern).

Clumped isotope paleotemperature estimates.

To quantitatively explore the relationship between climate and nacre biomineralization, we compared nacre analyses with independent estimates of paleotemperature. Carbonate clumped isotope thermometry provides an independent, thermodynamically-controlled measure of formation temperature (29). This geochemical method depends on the ordering of 13C-18O bonds within the carbonate lattice. Unlike the

δ18O paleothermometer, the carbonate clumped isotope thermometer does not require any assumptions about the δ18OVSMOW of precipitating water.

Carbonate clumped isotope analyses were completed on all of the modern and fossil specimens (Table S2). Since the method can be used on a range of minerals including

6 calcite and aragonite, where possible, both phases were separately sampled and analyzed from a single Pinna or Atrina shell. Because 8-10mg of carbonate is required for a single analysis, we sampled aragonite and calcite phases close to the PIC-mapped region (either across from it or immediately adjacent). Samples of calcite and aragonite from Ar5 were harvested from the opposite valve.

Clumped isotope results from the three modern pen shells compare well to buoy temperatures measured at each location (Figures S13-S15). Given the likelihood that the majority of the mass in these shells was formed over less than a year (8, 30, 31), small deviations from the mean annual temperature are not surprising. Calculated δ18OVSMOW values of precipitating seawater are positive and similar to measured δ18OVSMOW data from the evaporatively enriched Gulf of Mexico, Mediterranean Sea and tropical Caribbean Sea.

The modern temperature and δ18OVSMOW results validate the mean TT vs. temperature correlation and the clumped isotope temperature measurements of the fossil shells.

Reconstructed paleotemperatures for the fossil shells appear reasonable given their paleolatitudes and predicted climatic trends from other proxies (3). The Miocene specimens sit within the current range of seasonal temperatures from the Chesapeake Bay and Mid-Atlantic Coast. The Eocene specimens yield warmer mean temperature estimates

(16 ± 2.5°C and 21 ± 5°C), and the Cretaceous paleotemperature estimates are warmest and most similar to the modern specimen from tropical Panama (23 ± 3°C and 27 ± 4°C).

Nacre Tablet Thickness Quantitatively Reflects Paleotemperature

Figure 3 plots mean TT across the entire thickness of each pen shell against measured mean clumped isotope temperatures for the same shells. When all specimens

7 are included, the correlation coefficient is R = 0.83 (R2 = 0.69). The observation of such a strong correlation between mean TT and T, despite short-term fluctuations (Figure S12), indicates that long-term TT is thermodynamically constrained. Nacre, therefore, preserves a physical indication of carbonate formation temperature.

The empirical relationship between mean TT and T prompts the question of what mechanisms may underlie the correlation. To explore this further we experimentally measured abiotic aragonite growth rates at different temperatures over a standard time range. We measured the radii of growing aragonite spherulites, then averaged and plotted them as a function of growth T. The results confirm a linear, positive correlation of particle size with T, with a correlation coefficient R = 0.97 (R2 = 0.94) (Figure S16). The slope of the linear fit, however, is more than 100-fold greater in abiotic versus biotic growth (d(TT or

R)/d(temperature) = 1.531μm/˚C in synthetic aragonite vs. 0.012 μm/˚C measured in pen shells, Figures S16 and 3); hence, nacre deposition in animals proceeds at rates far lower than those allowed by simple crystal growth from solution. Importantly, however, the correlation is positive in both Figures 3 and S16. The comparison between synthetic and biogenic growth-T relationships does not exclude a biological influence on TT, but suggests that any such physiological signal does not obscure the primary signal imparted by thermodynamics.

Conclusions

We have demonstrated that pen shells record and preserve a quantitative indication of temperature in the thickness of nacre tablets formed during growth. We used PIC-maps to perform high-resolution measurements of tablet thickness, however, SEM images will

8 provide quick and easy access to the required TT data. All paleoenvironmental proxies have their strengths and weaknesses: temperature estimation from nacre TT requires good preservation of aragonite tablets, which are susceptible to dissolution; oxygen isotopes require a water reference and samples not altered during diagenesis; carbonate clumped isotope thermometry remains in its youth, and requires further calibration. The strength of this new proxy, however, complements the strengths and compensates for the weaknesses of previously proposed geochemical signatures, especially in the shallow marine environments that preserve most of the invertebrate fossil record. Continuing research on other fossil taxa will enable us to know to what extent the relationship shown in Figure 3 is taxon-specific. Importantly, however, by providing a simple and reliable physical means of estimating paleotemperature, nacre TT has the potential to establish an enhanced regional framework of climate and climatic variation that will illuminate changes in the abundance, diversity and geographic distribution of skeletonized marine animals over the past seventy million years.

Acknowledgements

We thank Andreas Scholl and Anthony Young for discussions and expert technical help during the experiments. We thank Nami Kitchen, Yunbin Guan and Chi Ma for help with analytical measurements at Caltech. We are indebted to Jessica Cundiff, Susan Butts,

Jessica Utrup, Neil Landman, Bushra Hussaini, Robert Hazen and John Nance for their assistance in finding and loaning fossil specimens used in this analysis. PG acknowledges support from the Radcliffe Institute for Advanced Study at Harvard University, NSF grant

DMR-1105167, DOE grant DE-FG02-07ER15899, US-Israel Binational Science Foundation

9 grant BSF-2010065. PEEM experiments were done at the ALS, supported by DOE grant DE-

AC02-05CH11231. AHK and CEM acknowledge support from the NASA Astrobiology

Institute and the NASA Postdoctoral Program. KB acknowledges support from the Harvard

Society of Fellows.

Figures and captions

10 Figure 1. PIC-maps of two Pinna shells samples, one modern (Pn1-1) and one from the

Late Cretaceous (Ps6-1), showing the prismatic calcite layer at the bottom (c) and aragonite nacre (a) at the top of each image, with dark organic layers separating them. The spectra on the right originate from ~2µm square locations in the shell, correspondingly labeled.

Figure 2. Nacre PIC-maps from the four geologic epochs in this study. Colors identify different c-axis crystal orientations (see color legend) and differentiate individual nacre 11 tablets, even in the presence of surface scratches (A: Modern) or missing fragments of nacre tablets (C: Eocene, D: Late Cretaceous).

Figure 3. The relationship between nacre tablet thickness (TT) and temperature (T). All

TTs in a shell cross-section are measured microscopically from PIC-maps as shown in

Figure S11 and S12, then d across each shell. T was independently measured with carbonate clumped isotope analysis from a shell fragment adjacent to the PIC-mapped area.

Error bars depict one standard deviation (of TT measurements) or one standard error of the mean (= 1σ/√n, where 1σ is the standard deviation of n clumped isotope analyses).

The red line shows the linear fit of the experimental data, obtained for TT = 0.322 + 0.012 T.

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