https://orcid.org/0000-0002-3148-4971
Figures
Abstract
Cephalopod carbonate geochemistry underpins studies ranging from Phanerozoic, global-scale change to outcrop-scale paleoecological reconstructions. Interpreting these data hinges on assumed similarity to model organisms, such as Nautilus, and generalization from other molluscan biomineralization processes. Aquarium rearing and capture of wild Nautilus suggest shell carbonate precipitates quickly (35 μm/day) in oxygen isotope equilibrium with seawater. Other components of Nautilus shell chemistry are less well-studied but have potential to serve as proxies for paleobiology and paleoceanography. To calibrate the geochemical response of cephalopod δ15Norg, δ13Corg, δ13Ccarb, δ18Ocarb, and δ44/40Cacarb to modern anthropogenic environmental change, we analyzed modern, historical, and subfossil Nautilus macromphalus from New Caledonia. Samples span initial human habitation, colonialization, and industrial pCO2 increase. This sampling strategy is advantageous because it avoids the shock response that can affect geochemical change in aquarium experiments. Given the range of living depths and more complex ecology of Nautilus, however, some anthropogenic signals, such as ocean acidification, may not have propagated to their living depths. Our data suggest some environmental changes are more easily preserved than others given variability in cephalopod average living depth. Calculation of the percent respired carbon incorporated into the shell using δ13Corg, δ13Ccarb, and Suess-effect corrected δ13CDIC suggests an increase in the last 130 years that may have been caused by increasing carbon dioxide concentration or decreasing oxygen concentration at the depths these individuals inhabited. This pattern is consistent with increasing atmospheric CO2 and/or eutrophication offshore of New Caledonia. We find that δ44/40Ca remains stable across the last 130 years. The subfossil shell from a cenote may exhibit early δ44/40Ca diagenesis. Questions remain about the proportion of dietary vs ambient seawater calcium incorporation into the Nautilus shell. Values of δ15N do not indicate trophic level change in the last 130 years, and the subfossil shell may show diagenetic alteration of δ15N toward lower values. Future work using historical collections of Sepia and Spirula may provide additional calibration of fossil cephalopod geochemistry.
Citation: Linzmeier BJ, Jacobson AD, Sageman BB, Hurtgen MT, Ankney ME, Masterson AL, et al. (2022) Isotope systematics of subfossil, historical, and modern Nautilus macromphalus from New Caledonia. PLoS ONE 17(12): e0277666. https://doi.org/10.1371/journal.pone.0277666
Editor: Lukas Jonkers, Universitat Bremen, GERMANY
Received: September 29, 2021; Accepted: November 1, 2022; Published: December 28, 2022
Copyright: © 2022 Linzmeier et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All stable isotope and elemental data are available in the Supplemental data file (SI 1) and are published in the EarthChem Library (https://doi.org/10.26022/IEDA/112707).
Funding: Ubben Program for Climate and Carbon Science at Northwestern University to BJL, ADJ, BBS, and MTH David and Lucile Packard Foundation (2007–31757) to ADJ The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Introduction
The geochemistry of cephalopod mollusks has been used to quantify paleoclimate [1,2] and investigate paleobiology [3–9] throughout their long fossil record [10]. Modern Nautilus is a model organism for the isotope geochemistry of extinct cephalopods, including the ammonoids and nautiloids, because it is the only remaining externally shelled cephalopod (Fig 1). Nautilus are forereef scavengers that cross hundreds of meters of water depth within individual days while continuously growing shell. Extensive work has been done to quantify the systematics of light stable isotopes (δ13C and δ18O) in Nautilus shell carbonate. Aquarium rearing experiments suggest Nautilus shells precipitate in δ18O equilibrium with seawater [11,12]. Carbon isotope values (δ13Cshell) suggest both metabolic and dissolved inorganic carbon (DIC) sources [11] similar to that for other mollusks [13]. Analyses of δ15N from shell organic matter, also known as conchiolin, show trophic change associated with hatching and maturity [14]. The carbon isotope value of conchiolin, like organic matter in other mollusk shells, likely reflects the δ13C of respired carbon [13,15,16].
Nautilus shells grow in a spiral and septa are secreted to allow for the maintenance of neutral buoyancy during growth through the removal of liquid from the chambers [17]. Shells comprise two major structural forms of aragonite, the inner nacreous layer and outer spherulitic prismatic layer [18,19].
Other isotope systems, particularly metal isotopes, have received less investigation. The calcium isotope value (δ44/40Ca) of Nautilus shell has only recently been measured from a handful of modern shells [20,21] and may reflect changing Nautilus fractionation factor (Δ44/40Cashell-SW [22], changing δ44/40Ca value of seawater [23], or dietary change [20,21].
Proxies respond to anthropogenic forcings of environmental change. Some of these shifts are particularly dramatic and likely to impact Nautilus, including the rise of coastal ‘dead zones’ [24], overfishing [25], and acidification [26]. For most organisms, these environmental changes are unfolding on a generational timescale, so phenotypic plasticity and ecosystem feedbacks may allow for faster adaptation, potentially mitigating the worst possible effects [27–30]; however, it is difficult to assess deep-time analogs for change on timescales of 100’s to 10,000’s of years due to the time-averaged and punctuated nature of the fossil record [31,32]. Careful, high precision analyses of proxies across modern to historical samples provide an opportunity to calibrate the geochemical changes expected in fossil archives and provide insight into variations expected to be preserved within fossil assemblages during abrupt climate events.
Here, we use museum collections to test for hypothesized anthropogenic forcings (e.g. temperature change, ocean acidification, trophic change) and diagenetic vulnerability present in a suite of analyses (Sr/Ca, Mg/Ca, δ13Corg, δ15Norg, δ13Ccarb, δ18Ocarb, and δ44/40Cacarb) of N. macromphalus from New Caledonia (Fig 2). Samples range in age from modern to subfossil and span indigenous settlement [33], European colonization, and industrial ocean acidification and warming (Fig 3). We hypothesize abrupt changes in ecologically sensitive proxies (e.g. δ18Ocarb, δ15Norg) are stepwise due to ecological restructuring, while gradual changes are forced due to continuous industrial environmental effects. These data highlight the utility of museum collections and the subfossil record for better quantifying past environmental change to predict biological resiliency in the face of anthropogenic pressures.
A) World map showing the location of New Caledonia in the Southwestern Pacific Ocean. B) Local map showing New Caledonia and the surrounding islands with a star indicating the location of the cenote. Water shallower than 1000 m is in light blue and approximates the habitat of N. macromphalus. around New Caledonia. All cenote specimens are from the star location of Lifou, Loyalty Islands [34]. All other specimens were collected near the large island and are recent museum specimens. Reliable accounts of the live collection of N. macromphalus are mostly known from areas close to New Caledonia, and the species is thought to have a geographic range restricted to that region [35]. Local currents are overlain for reference [36].
Red vertical bars represent the age of specimens used in this study with the museum repositories noted (American Museum of Natural History—AMNH, Field Museum of Natural History—FMNH, and Royal Ontario Museum—ROM). Yellow vertical bar represents indigenous settlement as demonstrated by landscape change observed in lacustrine sediments ~3000 BCE [33]. French invasion occurred in the mid-1800’s. The comparative record of pCO2 change showing industrial increases is from Law Dome, East Antarctica [37].
Materials and methods
Ethics statement
All specimens of N. macromphalus (Mollusca: Cephalopoda) used in this study were collected for morphological study of Nautilus and deposited at various museums (American Museum of Natural History, Field Museum of Natural History, Royal Ontario Museum). The methods of capture and sacrifice of Nautilus before the 2000’s specimens are unknown, but all specimens were collected before local protected status was granted in 2008. The two individuals collected in 2002 and 2004 were captured in a baited trap by Dr. Royal H. Mapes, sacrificed, and kept for a morphological study.
Nautilus macromphalus samples
N. macromphalus is endemic to New Caledonia and the Loyalty Islands and can be distinguished by the prominent, open umbilicus with inward sloping walls ([38], Fig 1). Individual Nautilus likely grow to maturity over 2.5 to 6 years, although considerable uncertainty remains in their total lifespan [39]. The oldest samples used in this study are AMNH 112600 and AMNH 112595. These samples were recovered from a cenote on Lifou (Fig 2) and date to 6455 ±30 (AMNH 112600) and 6895 ±30 (AMNH 112595) years before present using radiocarbon [34]. Multiple fragments from near the aperture of this shell were powdered to provide adequate material for analyses. The second oldest sample is from the Field Museum of Natural History in Chicago (FM 41) and was part of the original collection purchased from Wards Scientific to start the collection after the World’s Columbian Exposition in 1893. A single 2 cm2 chip from near the aperture was removed for analysis. Three samples from the Royal Ontario Museum (ROM 60177, 48997, and 49000) were collected in 1975, 1977, and 1978 respectively. Small chips of approximately 2 cm2 were removed from the aperture. The most recent samples, housed at the American Museum of Natural History (AMNH 105621, AMNH 123397), were collected in 2002 and 2004, respectively. One sample, AMNH 105621, was previously studied for δ18Ocarb variability by secondary ion mass spectrometry [12]. For this sample, powder was drilled from a chip that was embedded in epoxy.
Organic matter δ13C and δ15N
Processing of carbonate to extract organic matter was done in the Sedimentary Geochemistry Laboratory at Northwestern University. Powdered shell was reacted with room temperature 1 N HCl overnight. Smaller amounts of recent shells with abundant organic matter were reacted with smaller volumes of HCl necessary for complete dissolution and then dried down to isolate the organic matter. The subfossil shells from the cenote required ~1–2 g of shell for the analyses presented here. Organic matter was collected from solution using ashed glass filters. Either organic matter or organic matter plus filters were loaded into tin capsules and combusted at 980 ⁰C on a Costech 4010 Elemental Analyzer, coupled to a ThermoFinnigan Delta V Plus mass spectrometer via a ConFlo IV interface in the Stable Isotope Laboratory at Northwestern University. Long term precision of δ13C and δ15N analyses (±0.4‰ and ±0.6‰, 2σSD) was assessed by comparison with isotope standards IU acetanilide (δ13C = -29.52±0.02‰, δ15N = +1.18‰) and IU urea (δ13C = -8.02±0.05‰, δ15N = +20.17±0.06‰) supplied by Indiana University [40]. This method of measurement does not distinguish between carbonate-bound organic matter (intracrystalline) and non-carbonate bound organic matter (intercrystalline) but produces average δ13C and δ15N values for all organic matter isolated from the Nautilus shell.
Carbonate δ13C and δ18O
Analyses of carbonate powder were conducted in the Stable Isotope Laboratory at Northwestern University using a Thermo Gasbench II coupled with continuous flow of He carrier gas to a Thermo Delta V IRMS. Values were standardized to the Vienna Pee Dee Belemnite (VPDB) scale using NBS-18 (National Bureau of Standards, δ18O = -23.2 ‰, δ13C = -5.01 ‰, VPDB) and an in-house carbonate standard, Carrara Lago Marble (CLM δ18O = -3.66 ‰, δ13C = 2.31 ‰, VPDB). The CLM standard has been calibrated alongside NBS-19 and IAEA-603. A two-point calibration using CLM and NBS-18 was employed for the analyses presented here. Analytical uncertainties (2σSD) for these analyses are ±0.2‰ for δ18Ocarb and ±0.1‰ for δ13Ccarb.
Elemental analysis
Approximately 50 mg of powdered shell was placed in acid-washed HDPE test tubes and dissolved in ~10 mL of 5 wt% HNO3. The mixtures were agitated on a rocker table for ~24 hours, centrifuged, and then filtered through 0.45 μm syringe filters. Solutions were diluted with 5 wt% HNO3 to ensure elemental concentrations were within calibration ranges of standards (assuming near-to-pure calcium carbonate). Measurements were done using a Thermo Scientific iCAP 6500 ICP-OES using Argon carrier gas and a Cetac U-6000AT+ Ultrasonic Nebulizer in the Aqueous Geochemistry Laboratory at Northwestern University. Repeated measurements of NIST SRM 1643f were used to both monitor instrument stability and confirm data quality for Ca, Mg, Mn, Na, and Sr. Three replicates of 3mL of solution were averaged for standards, blanks, and samples. Instrument drift was monitored using a standard, sample, standard bracketing technique with no more than 15 samples analyzed between standards. Standard measurements suggest an instrumental precision of ±5% (RSD, relative standard deviation) for each element (Ca ~0.5 ppm, Mg ~0.1 ppb, Mn ~0.1 ppb, Na ~6 ppb, and Sr ~5 ppb).
Carbonate δ44/40Ca
Calcium isotope values were measured in the Radiogenic Isotope Laboratory at Northwestern University using an optimized 43Ca-42Ca double spike method implemented on a Thermo-Fisher Triton Multi-Collector Thermal Ionization Mass Spectrometer (TIMS) [41]. Sample solutions containing 50 μg of Ca were weighed into acid-cleaned Teflon vials, spiked, and equilibrated. Solutions were dried down overnight at 90°C. Residues were then dissolved in 0.5 mL of 1.55N HCl, and Ca was separated from other elements by passing solutions through Teflon columns filled with Bio-Rad AG MP-50 cation exchange resin. Solutions were dried down once more and subsequently treated with two drops of 35 wt% H2O2 to oxidize organic compounds and finally two drops of 16N HNO3 to convert Ca to nitrate form. Samples were then dissolved in 0.4 μL of 8N HNO3 and split into 4 beads. One bead was loaded onto a single degassed tantalum filament assembly, between ~0.5 mm wide parafilm dams, and subsequently dried at 3.5 amperes after adding 0.5 μL of 10 wt% H3PO4.
A stable, 20V 40Ca ion beam was obtained after a 0.5 hr warm-up sequence. Measurement of 40Ca/42Ca, 43Ca/42Ca, and 43Ca/44Ca ratios was accomplished using a three-hop collector cup configuration. Sample (SMP) 44Ca/40Ca ratios are reported in delta notation relative to OSIL seawater (SW), where δ44/40CaSMP = [(44Ca/40Ca)SMP / (44Ca/40Ca)SW− 1] x 1000. Analyses of the OSIL SW standard yielded a reproducibility of ±0.04‰ (2σSD) during the analytical sessions including these samples. Analyses of NIST 915b produced an average δ44/40Ca value of -1.14‰ ± 0.07‰ (2σSD) during the duration of the study. All stable isotope and elemental data are available in the S1 Data and are published in the EarthChem Library (https://doi.org/10.26022/IEDA/112707).
Difference estimates
The difference estimates between smaller subsets of data are based on a Monte Carlo approach. We add a random error term to each analysis assuming the instrumental precision describes two standard deviations of a normal distribution for expected variability around our measured values. We then calculate the difference between groups for this new dataset and repeat this operation 1,000,000 times. Error estimates are reported as the 5th to 95th percentiles of the differences between the groups from the Monte Carlo method.
Results
Carbonate trace elements
Recent samples show no discernible temporal trends in either Mg/Ca or Sr/Ca ratios and display similar variation to the subfossil specimens (Fig 4). Material from subfossil cenote specimens has higher Sr/Ca (3.0 mmol/mol) and lower Mg/Ca (0.5 mmol/mol) than most historical samples (Fig 4).
Error bars are 2 standard deviation instrumental precision for isotope values and the 5% RSD propagated to the elemental ratios. A) δ44/40Ca vs Mg/Ca, B) δ44/40Ca vs Sr/Ca, C) δ13Cshell vs Mg/Ca, D) δ13Cshell vs Sr/Ca, E) δ18Oshell vs Mg/Ca, F) δ18Oshell vs Mg/Ca, G) δ15N vs Mg/Ca, H) δ15N vs Sr/Ca, I) δ13Corg vs Mg/Ca, and J) δ13Corg vs Sr/Ca. The cenote and historical samples distinctly differ along Mg/Ca, Sr/Ca, δ15N, δ13Corg, and δ44/40Ca axes.
Carbonate isotopes
The cenote specimens fall within the range of δ18O and δ13C of shell carbonate measured for modern specimens (Fig 5). No change in δ44/40Ca is apparent in these samples less than 120 years old; however, the subfossil cenote specimens are 0.12‰ lower (0.11 to 0.15‰) than modern samples (Fig 6A). For samples collected in the last 120 years, δ13Cshell decreases by 2.09‰ (2.03 to 2.15‰) toward the present (Fig 6B), while δ18Oshell increases by 0.32‰ (0.45–0.20‰) (Fig 6C).
Error bars are 2 standard deviation instrumental precision.
Error bars are 2 standard deviation instrumental precision. A) Shell δ44/40Ca through time. B) The δ13C of shell carbonate through time. C) The δ18O of shell carbonate through time. D) The δ15N of shell organic matter though time. E) The δ13C of shell organic matter through time.
Organic matter isotopes
Samples spanning the last 130 years show no temporal trends in either δ13Corg or δ15Norg (Figs 6D, 6E and 7). Subfossil cenote specimens have lower δ13Corg and δ15Norg by 6.06‰ (6.25 to 5.87‰) and 1.74‰ (2.03 to 1.45‰), respectively. Recent samples also consistently have lower C/N (<3) compared to subfossil specimens (>4, Fig 7B).
Error bars are 2 standard deviation instrumental precision. A) δ13Corg vs δ15Norg, B) C/N vs δ15Norg.
Discussion
Diagenesis
Elemental ratios.
Elemental ratios of biogenic carbonates are vulnerable to diagenetic alteration. Increases in Sr/Ca from 2 mmol/mol to 5 mmol/mol have been correlated with microstructural diagenetic alteration of fossil cephalopod shell and correspond to change in 87Sr/86Sr, δ18Ocarb, and δ13Ccarb. The cenote samples do not appear to be outliers in either Sr/Ca or Mg/Ca compared to modern samples, however. This suggests that diagenetic alteration of Sr/Ca and Mg/Ca is not detectable in the cenote samples.
Organic matter isotopes.
Although organic matter within mollusk shells has been reported for multiple fossil specimens, pristine preservation is rare [42–45]. During dissolution of these shells for isolation of organic matter, it is apparent that cenote specimens have considerably less organic matter than modern specimens, but the effects on the isotope composition of residual organic matter is important to explore. Degradation of organic matter within shells generally removes more labile organic matter (e.g. amino acids, glycoproteins, sugars) and preserves refractory organic matter, although the exact effect on δ13Corg and δ15Norg values is unknown. Two sources of organic matter in the shell, carbonate-bound organic matter (intracrystalline) and non-carbonate bound organic matter (intercrystalline), likely behave differently during diagenesis due to the differing volumes and connectedness of the organic matter for microbial degradation. Some authors have noted much lower δ15N (1–4‰) in significantly older fossil nautiloids (Cymatoceras sakalavus, Albian ~113 to 100 Ma) and have suggested these low δ15N values reflect diagenetic alteration [14]. Sedimentary organic matter degradation drives δ15N toward lower values while C/N increases [46]. We see a similar pattern between the recent and subfossil specimens (Fig 7B) and therefore suggest that the δ15N of the cenote specimens is altered and does not reflect a primary trophic level signature. The δ13Corg values in these samples are also lower than the more recent specimens (Fig 7A). Diagenetic alteration of δ13Corg in mollusks also likely drives isotope values lower due to a loss of the hydrophilic fraction of organic matter and potentially transformation to hydrophobic organic matter. The transformation involves preferentially losing 13C by not reincorporating it in hydrophobic organic matter.
Carbonate isotopes.
Diagenetic alteration of light stable isotopes is of particular interest for constraining the fidelity of paleoclimatological records [47–49]. The subfossil specimens from the cenote show signs that shell nacre recrystallized [34], and higher Sr/Ca in these shells is consistent with addition of either strontianite [47] or authigenic aragonite (Fig 4B). The lack of clear δ13C or δ18O outliers is notable and suggests that any recrystallization did not incorporate large volumes of additional diagenetic carbonate. Shell δ44/40Ca may have been altered toward lower values, as has been observed in Cretaceous mollusks from Antarctica [22], where trends toward higher Sr/Ca (5 up to 12 mmol/mol) correlate with lower δ44/40Ca values (from -1.5 to -2‰). This could point to the addition of small domains of authigenic aragonite or strontianite, but the variation observed in the Sr/Ca in the most recent N. macromphalus (Fig 4) suggests that the pattern may not be consistent with diagenesis.
If any diagenesis occurred, it happened at low temperatures (~28°C), ambient pressures, and within the last 7000 years [34] given the location of the cenote and previously published radiocarbon ages. Carbonate recrystallization/precipitation was likely tied to microbial degradation of organic matter causing variable carbonate saturation state within or near shells [50,51]. Future work contrasting these diagenetic pathways with higher temperature hydrothermal experiments [52,53] may help provide a more detailed ‘taphonomic chronometer’ for use in deep time [54].
Isotope and elemental interpretation
Elemental ratios.
The elemental ratios of Nautilus shells potentially reflect taxonomic or geographic differences rather than temperatures, as has been observed in bivalve mollusks. We observe a wide range of Sr/Ca and Mg/Ca across these samples with no clear trend towards modern samples. This variation within modern specimens suggests that more work on Mg/Ca and Sr/Ca variation within Nautilus is needed to understand the limits of intraspecific variation and potential thresholds for identification of diagenetic alteration.
Organic matter isotopes.
Modern and historical shells suggest slight variation in prey preference or availability for the individuals measured (Fig 7A). In other work on Nautilus, δ15Norg changes with hatching and early growth and variation of ~1–2‰ within and between individuals has been observed [14]. Similar individual–to–individual and within individual variability may be linked to differing prey choice [55,56] and is likely to be present in Nautilus given neurological complexity [57]. There are no strong trends through time in the recent δ13Corg or δ15Norg (Figs 6D, 6E and 7A) that would suggest major trophic changes for these N. macromphalus in the last ~120 years. Future work using compound specific δ15Norg analysis of amino acids within samples like these could support trophic level stability.
Calcium isotopes.
Previous studies have proposed that δ44/40Ca can indicate trophic level for vertebrates in modern and ancient terrestrial and marine ecosystems [58,59]. Ingestion of hard tissue material and subsequent use of calcium from that source in biomineralization is likely necessary to cause a δ44/40Ca trophic level effect [60]. It is possible that the difference measured between the oldest N. macromphalus and the more recent samples (Figs 6A and 8F) reflects changing composition of scavenged prey, including crustaceans and fish [61], perhaps due to ecosystem changes coupled to fishing pressures [62,63]. Shifting dietary composition causing different δ44/40Ca is an unlikely explanation, however, because no strong correlation with either δ15Norg or δ13Corg is observed, and moreover, recent individuals show measurable differences in both isotope systems indicative of differing diets (Fig 8F [55]). In addition, comparing δ44/40Ca to average δ15N and trophic level across other modern Nautilus, Sepia, and Spirula suggests a lack of trophic response in cephalopods [21].
Error bars are 2 standard deviation instrumental precision. A) δ13Corg vs δ13Cshell, B) δ15N vs δ13Cshell, C) δ13Corg vs δ18Oshell, D) δ15N vs δ18Oshell, E) δ13Corg vs δ44/40Ca, and F) δ15N vs δ44/40Ca.
The calcium isotope composition of mollusk material may vary with the calcium isotope composition of seawater (δ44/40CaSW) or changes in the fractionation between seawater and precipitated shell (Δ44/40CaSW-Shell) [22]. Bivalve mollusks derive ~80% or more of their shell calcium from seawater sources [64] and can make use of only water sources for 100% of calcium in shell precipitation [65]. While shifts in local-scale Ca cycling dynamics are possible [23], changes in the isotopic composition of the global ocean unlikely explain the observed variations, given the long residence time of Ca in seawater. Evidence from the geologic record, however, suggests that Δ44/40CaSW-Shell is sensitive to seawater carbonate state. Culturing experiments show that the pH of extrapallial fluid from Arctica islandica bivalves is at least partially regulated during shell formation, but can vary with ambient pH [66]. If Nautilus similarly regulates the pH and potentially the saturation state of extrapallial fluid during shell precipitation, then variation in Δ44/40CaSW-Shell would be driven by mass-dependent isotope effects during transport into the extrapallial fluid rather than with varying saturation state and precipitation rate at the site of precipitation, as has been observed in inorganic systems. Temperature may affect Δ44/40CaSW-Shell in bivalves [67], although temperature covaries with carbonate saturation state, which can be modulated by the ratio of photosynthesis to respiration [68,69], and in general, the temperature sensitivity of Δ44/40CaSW-Shell for other carbonate producers is low [20,70–73].
Seawater likely constitutes the largest source of calcium for the precipitation of N. macromphalus shell [64,65], but complex precipitation and resorption of intermediate carbonate reservoirs could influence shell δ44/40Ca [74]. Uroliths represent one proposed intermediary carbonate structure between seawater and shell precipitation [75]. These structures are amorphous calcium phosphate and have higher Sr contents than the shell wall [76]. The calcium fractionation factor for this material is unknown, but may be close to -1‰, similar to peloidal calcium phosphate [77,78].
Fixed Δ44/40CaSW-Shell in cephalopods (mostly for belemnites) is typically assumed in the reconstruction of δ44/40CaSW change through time [21,79–81]. Recent evidence suggests that Δ44/40CaSW-Shell for other types of carbonate producers varies with seawater saturation state [22,82,83] in a way consistent with theoretical models for inorganic calcite formation [84,85]. Any variation of cephalopod Δ44/40CaSW-Shell may reflect additional controls, such as changes in the transport of Ca into the extrapallial fluid (EPF). One possibility is that proportions of Ca transported by selective intracellular calcium channels, non-selective intercellular pathways, or active enzymatic transport (Ca2+-ATPase and carbonic anhydrase) can change. However, under most conditions, selective intracellular calcium channels are thought to dominate transportation of Ca into the EPF through high diffusive fluxes that are selective for Ca [86]. Another possibility is that any Ca isotope fractionation imparted by one or more of these transport mechanisms varies with seawater saturation state. Future well-controlled aquarium rearing experiments will be necessary to determine if Δ44/40CaSW-Shell changes with carbonate saturation state or another environmental condition.
For anthropogenic ocean acidification to change Δ44/40Ca of these Nautilus, higher CO2 concentrations must propagate to their living depths, which in turn must remain relatively stable throughout the study interval. The observed change in δ13C of shell carbonate (Fig 6B) suggests propagation of anthropogenic carbon into the habitat of the Nautilus but does not guarantee a change in the concentration of CO2 necessary to cause acidification. Boron isotope measurements from shallow water (7–8 m) coral suggests a decrease of ~0.15 pH near New Caledonia since the 1890’s, but also indicate similar variations on decadal timescales [87]. Deeper waters, like those that the Nautilus inhabit, are generally expected to acidify more slowly, although organic matter export can sometimes enhance acidification at depth depending on the interaction between deep water ventilation, organic matter export, and general ocean circulation patterns [88,89]. Because the oceans are still in the early stages of acidification, it is likely that the amount of pH change at these depths has not been sufficient to cause detectable alteration in the δ44/40Ca of the studied Nautilus specimens.
Respired CO2.
The proportion of respired carbon incorporated into the shells of mollusks depends on changes in ambient O2:CO2 in surrounding waters [13,90] and the metabolic rate [91]. Use of the proxy assumes that all carbon used for the precipitation of biogenic carbonates derives from either seawater dissolved inorganic carbon (DIC) or respired CO2 derived from food. The δ13C metabolic rate proxy has been explored using aquarium-reared cephalopods, including Sepia pharaonis [92,93]. The proportion of respired carbon contributing to carbonate precipitation can be calculated following a simple relationship outlined by [13,90]:
(1)
Where δ13Cshell refers to the measured value for carbonate shell material. We assume δ13Cmetabolic is equivalent to δ13Corg measured in the shell organic matter—given similar findings for other mollusks [16]. The value of εaragonite is assumed to be 2.7‰, which is the value for inorganic aragonite [94]. To constrain δ13CDIC, we use published estimates of δ13CDIC for preindustrial (1.2‰, VPDB) and recent (1.0‰, VPDB) water near New Caledonia [95,96] at the average N. macromphalus living depth of ~400 m [97]. This depth is chosen even though shell grows across a range of at least 400 m water depth [12] due to time averaging of bulk samples like those used in this study [98]. We assume no ontogenetic change in δ13Ccarb biases our results. All samples were from near at the aperture of the body chamber of large shells, and most change in δ13Ccarb has been observed in the shell near to hatching rather than later in ontogeny, as is observed in bivalves.
Calculations using these metrics show increasing amounts of respired carbon are being incorporated into the shells of N. macromphalus during the last 130 years (Fig 9). The observed increase (from ~8 to ~22%) likely reflects changing metabolic rates caused by transgenerational acclimation to ocean acidification, as has been seen in Mya arenaria bivalves [91]. The increase is much less than the observed metabolic carbon increase (27% to 61%) in the experimentally reared bivalves over what is likely to be a much larger pH range (8.1 to 7.7 pH) [91]. Other experimentation with Arctica islandica bivalves has suggested that ontogenetic variation in the amount of respired carbon incorporated into shells is minimal [99]. Because the Nautilus live relatively deep, CO2 incorporation from the atmosphere is likely to be lower than that experienced by shallower organisms. The decrease of pH at the living depths of these N. macromphalus may be facilitated by dampened deep water oxygenation related to continued organic matter export [88]. The observed increase in respired carbon could also be modulated by changes in the ratio of dissolved oxygen to carbon dioxide through expanding oxygen minimum zones offshore of New Caledonia due to increased agricultural intensity and nutrient-rich runoff [100,101], dramatic changes to vegetation [102], increasing [CO2] due to anthropogenic injection into the atmosphere-ocean system [103], pressure from mining runoff [104], or changing preferred habitat depths due to changing ecosystem composition from fishing other organisms (Fig 3). It is also unlikely that the observed increase in metabolic carbon is caused by ontogenetic change (e.g., because shells represent mature Nautilus and most δ13Ccarb change occurs very early in ontogeny.
Note the increase in the amount of metabolic carbon incorporated into the shell since the 1970’s.
Future work
One of the primary challenges to clearly calibrating geochemical proxies in biogenic carbonates is the ‘shock’ of changing environmental conditions during the experimental treatment of individuals [105,106]. Although the magnitude of anthropogenic and natural environmental change can be large, both are slow relative the generational timescale of organisms. This means that the best calibrations for proxies preserved in biogenic carbonates may be found in historical or spatially distributed samples that inhabited conditions across several generations [29,105]. Studies in modern settings may benefit from cross-calibration with low-cost real-time environmental logging [107]. Focus on mollusk shell is of particular merit due to wide ranging methods for diagenetic assessment [47,48,53,108,109] and preservation of shell organic matter [43,44]. Future work on these isotope systems in cephalopods and other mollusks should leverage museum collections spanning collection time and geographic range to avoid confounding factors of shock and to allow for adaptive responses. Further work on internally shelled mollusks (Sepia and Spirula) may be informative for interrogating belemnite archives given newfound microstructural complexity [110,111].
Conclusions
Geochemical analyses of subfossil, historical, and modern N. macromphalus show the importance of calibrating geochemical signals across generations of organisms. The low temperature, potential diagenetic alteration also points to the importance of robust diagenetic assessment of samples from different environments. Our data suggest that there is intergenerational increase in N. macromphalus metabolism near New Caledonia, which is likely caused by ocean acidification. Future work using historical and modern marine mollusk shell material will be important for calibrating geochemical proxies across events that can cause both selection and/or phenotypic plasticity response.
Supporting information
S1 Data. Spreadsheet with all analytical data for all samples.
Each tab contains one group of analyses.
https://doi.org/10.1371/journal.pone.0277666.s001
(XLSX)
Acknowledgments
We would like to thank Jochen Gerber (Field Museum) and Bushra Hussaini (AMNH) for assistance in accessing samples. We also thank three anonymous reviewers for their constructive comments to improve this manuscript.
References
- 1. Price GD, Twitchett RJ, Wheeley JR, Buono G. Isotopic evidence for long term warmth in the Mesozoic. Sci Rep. 2013;3. pmid:23486483
- 2. Urey HC, Lowenstam HA, Epstein S, McKinney CR. Measurement of paleotemperatures and temperatures of the Upper Cretaceous of England, Denmark, and the Southeastern United States. GSA Bull. 1951;62: 399–416.
- 3. Ellis NM, Tobin TS. Evidence for seasonal variation in δ13C and δ18O profiles of Baculites and implications for growth rate. Palaeontology. 2019;62: 583–598.
- 4. Ferguson K, Macleod KG, Landman NH, Sessa JA. Evaluating growth and ecology in baculitid and scaphitid ammonites using stable isotope sclerochronology. PALAIOS. 2019;34: 317–329.
- 5. Landman NH, Cochran JK, Slovacek M, Larson NL, Garb MP, Brezina J, et al. Isotope sclerochronology of ammonites (Baculites compressus) from methane seep and non-seep sites in the Late Cretaceous Western Interior Seaway, USA: Implications for ammonite habitat and mode of life. Am J Sci. 2018;318: 603–639.
- 6. Linzmeier BJ, Landman NH, Peters SE, Kozdon R, Kitajima K, Valley JW. Ion microprobe–measured stable isotope evidence for ammonite habitat and life mode during early ontogeny. Paleobiology. 2018;44: 684–708.
- 7. Lukeneder A, Harzhauser M, Müllegger S, Piller WE. Ontogeny and habitat change in Mesozoic cephalopods revealed by stable isotopes (δ18O, δ13C). Earth Planet Sci Lett. 2010;296: 103–114.
- 8. Moriya K, Nishi H, Kawahata H, Tanabe K, Takayanagi Y. Demersal habitat of Late Cretaceous ammonoids: Evidence from oxygen isotopes for the Campanian (Late Cretaceous) northwestern Pacific thermal structure. Geology. 2003;31: 167–170.
- 9. Sessa JA, Larina E, Knoll K, Garb M, Cochran JK, Huber BT, et al. Ammonite habitat revealed via isotopic composition and comparisons with co-occurring benthic and planktonic organisms. Proc Natl Acad Sci. 2015;112: 15562–15567. pmid:26630003
- 10. Kröger B, Vinther J, Fuchs D. Cephalopod origin and evolution: A congruent picture emerging from fossils, development and molecules. BioEssays. 2011;33: 602–613. pmid:21681989
- 11. Landman NH, Cochran JK, Rye DM, Tanabe K, Arnold JM. Early life history of Nautilus: evidence from isotopic analyses of aquarium-reared specimens. Paleobiology. 1994;20: 40–51.
- 12. Linzmeier BJ, Kozdon R, Peters SE, Valley JW. Oxygen isotope variability within Nautilus shell growth bands. PLOS ONE. 2016;11: e0153890. pmid:27100183
- 13. McConnaughey TA, Gillikin DP. Carbon isotopes in mollusk shell carbonates. Geo-Mar Lett. 2008;28: 287–299.
- 14.
Kashiyama Y, Ogawa NO, Chikaraishi Y, Kashi N, Sakai S, Tanabe K, et al. Reconstructing the life history of modern and fossil nautiloids based on the nitrogen isotopic composition of shell organic matter and amino acids. In: Tanabe K, Shigeta Y, Sasaki T, Hirano H, editors. Cephalopods—Present and Past. Tokyo: Tokai University Press; 2010. pp. 67–75.
- 15. Crocker KC, DeNiro MJ, Ward PD. Stable isotopic investigations of early development in extant and fossil chambered cephalopods I. Oxygen isotopic composition of eggwater and carbon isotopic composition of siphuncle organic matter in Nautilus. Geochim Cosmochim Acta. 1985;49: 2527–2532.
- 16. Gillikin DP, Lorrain A, Meng L, Dehairs F. A large metabolic carbon contribution to the δ13C record in marine aragonitic bivalve shells. Geochim Cosmochim Acta. 2007;71: 2936–2946.
- 17. Ward PD. Periodicity of chamber formation in chambered cephalopods: Evidence from Nautilus macromphalus and Nautilus pompilius. Paleobiology. 1985;11: 438–450.
- 18. Mutvei H. Ultrastructural relationships between the prismatic and nacreous layers in Nautilus (Cephalopoda). Biomineralization. 1972;4: 81–86.
- 19. Mutvei H. On the shells of Nautilus and Spirula: with notes on shell secretion in non-cephalopod molluscs. Ark För Zool. 1964;16: 221–278.
- 20.
Gussone N, Heuser A. Biominerals and Biomaterial. Calcium Stable Isotope Geochemistry. Berlin, Heidelberg: Springer Berlin Heidelberg; 2016. pp. 111–144. https://doi.org/10.1007/978-3-540-68953-9_4
- 21. Hoffmann R, Riechelmann S, Liebetrau V, Eisenhauer A, Immenhauser A. Calcium isotope values of modern and fossil cephalopod shells–Trophic level or proxy for seawater geochemistry? Chem Geol. 2021;583: 120466.
- 22. Linzmeier BJ, Jacobson AD, Sageman BB, Hurtgen MT, Ankney ME, Petersen SV, et al. Calcium isotope evidence for environmental variability before and across the Cretaceous-Paleogene mass extinction. Geology. 2020;48: 34–38.
- 23. Holmden C, Papanastassiou DA, Blanchon P, Evans S. δ44/40Ca variability in shallow water carbonates and the impact of submarine groundwater discharge on Ca-cycling in marine environments. Geochim Cosmochim Acta. 2012;83: 179–194.
- 24. Fennel K, Testa JM. Biogeochemical Controls on Coastal Hypoxia. Annu Rev Mar Sci. 2019;11: 105–130. pmid:29889612
- 25. Barord GJ, Dooley F, Dunstan A, Ilano A, Keister KN, Neumeister H, et al. Comparative Population Assessments of Nautilus sp. in the Philippines, Australia, Fiji, and American Samoa Using Baited Remote Underwater Video Systems. PLoS ONE. 2014;9: e100799. pmid:24956107
- 26. Doney SC, Fabry VJ, Feely RA, Kleypas JA. Ocean Acidification: The Other CO2 Problem. Annu Rev Mar Sci. 2009;1: 169–192. pmid:21141034
- 27. Kroeker KJ, Kordas RL, Harley CDG. Embracing interactions in ocean acidification research: confronting multiple stressor scenarios and context dependence. Biol Lett. 2017;13: 20160802. pmid:28356409
- 28. Schunter C, Welch MJ, Nilsson GE, Rummer JL, Munday PL, Ravasi T. An interplay between plasticity and parental phenotype determines impacts of ocean acidification on a reef fish. Nat Ecol Evol. 2018;2: 334–342. pmid:29255298
- 29. Telesca L, Peck LS, Backeljau T, Heinig MF, Harper EM. A century of coping with environmental and ecological changes via compensatory biomineralization in mussels. Glob Change Biol. 2021;27: 624–639. pmid:33112464
- 30. Urban MC, Bocedi G, Hendry AP, Mihoub J-B, Pe’er G, Singer A, et al. Improving the forecast for biodiversity under climate change. Science. 2016;353. pmid:27609898
- 31. Kidwell SM. Time-averaged molluscan death assemblages: Palimpsests of richness, snapshots of abundance. Geology. 2002;30: 803–806.
- 32. Kowalewski M, Casebolt S, Hua Q, Whitacre KE, Kaufman DS, Kosnik MA. One fossil record, multiple time resolutions: Disparate time-averaging of echinoids and mollusks on a Holocene carbonate platform. Geology. 2018;46: 51–54.
- 33. Stevenson J, Dodson JR, Prosser IP. A late Quaternary record of environmental change and human impact from New Caledonia. Palaeogeogr Palaeoclimatol Palaeoecol. 2001;168: 97–123.
- 34. Landman NH, Mapes RH, Cochran JK, Lignier V, Hembree DI, Goiran C, et al. An unusual occurrence of Nautilus macromphalus in a cenote in the Loyalty Islands (New Caledonia). PLOS ONE. 2014;9: e113372. pmid:25470257
- 35.
House MR. Geographic Distribution of Nautilus Shells. In: Saunders WB, Landman NH, editors. Nautilus: The Biology and Paleobiology of a Living Fossil, Reprint with additions. Dordrecht: Springer Netherlands; 2010. pp. 53–64. https://doi.org/10.1007/978-90-481-3299-7_4
- 36. Cravatte S, Kestenare E, Eldin G, Ganachaud A, Lefèvre J, Marin F, et al. Regional circulation around New Caledonia from two decades of observations. J Mar Syst. 2015;148: 249–271.
- 37. Etheridge DM, Steele LP, Langenfelds RL, Francey RJ, Barnola JM, Morgan VI. Historical CO2 records from the Law Dome DE08, DE08-2, and DSS ice cores. Trends Compend Data Glob Change. 1998; 351–364.
- 38.
Saunders WB. The Species of Nautilus. Nautilus. Springer, Dordrecht; 2010. pp. 35–52. https://doi.org/10.1007/978-90-481-3299-7_3
- 39.
Landman NH, Cochran JK. Growth and Longevity of Nautilus. Nautilus. Springer, Dordrecht; 2010. pp. 401–420. https://doi.org/10.1007/978-90-481-3299-7_28
- 40. Schimmelmann A, Albertino A, Sauer PE, Qi H, Molinie R, Mesnard F. Nicotine, acetanilide and urea multi-level 2H-, 13C- and 15N-abundance reference materials for continuous-flow isotope ratio mass spectrometry. Rapid Commun Mass Spectrom. 2009;23: 3513–3521. https://doi.org/10.1002/rcm.4277.
- 41. Lehn GO, Jacobson AD, Holmden C. Precise analysis of Ca isotope ratios (δ44/40Ca) using an optimized 43Ca–42Ca double-spike MC-TIMS method. Int J Mass Spectrom. 2013;351: 69–75.
- 42. Buchardt B, Weiner S. Diagenesis of aragonite from Upper Cretaceous ammonites: a geochemical case-study. Sedimentology. 1981;28: 423–438.
- 43. Clark GRI. Organic matrix taphonomy in some molluscan shell microstructures. Palaeogeogr Palaeoclimatol Palaeoecol. 1999;149: 305–312.
- 44. Myers CE, Bergmann KD, Sun C-Y, Boekelheide N, Knoll AH, Gilbert PUPA. Exceptional preservation of organic matrix and shell microstructure in a Late Cretaceous Pinna fossil revealed by photoemission electron spectromicroscopy. Geology. 2018;46: 711–714.
- 45. Weiner S, Lowenstam HA, Hood L. Characterization of 80-million-year-old mollusk shell proteins. Proc Natl Acad Sci. 1976;73: 2541–2545. pmid:785470
- 46. Junium CK, Arthur MA. Nitrogen cycling during the Cretaceous, Cenomanian-Turonian Oceanic Anoxic Event II. Geochem Geophys Geosystems. 2007;8.
- 47. Cochran JK, Kallenberg K, Landman NH, Harries PJ, Weinreb D, Turekian KK, et al. Effect of diagenesis on the Sr, O, and C isotope composition of Late Cretaceous mollusks from the Western Interior Seaway of North America. Am J Sci. 2010;310: 69–88.
- 48. Immenhauser A, Schöne BR, Hoffmann R, Niedermayr A. Mollusc and brachiopod skeletal hard parts: Intricate archives of their marine environment. Sedimentology. 2016;63: 1–59.
- 49. Swart PK. The geochemistry of carbonate diagenesis: The past, present and future. Sedimentology. 2015;62: 1233–1304.
- 50. Eyre BD, Cyronak T, Drupp P, Carlo EHD, Sachs JP, Andersson AJ. Coral reefs will transition to net dissolving before end of century. Science. 2018;359: 908–911. pmid:29472482
- 51. Ries JB, Ghazaleh MN, Connolly B, Westfield I, Castillo KD. Impacts of seawater saturation state (ΩA = 0.4–4.6) and temperature (10, 25°C) on the dissolution kinetics of whole-shell biogenic carbonates. Geochim Cosmochim Acta. 2016;192: 318–337.
- 52. Milano S, Prendergast AL, Schöne BR. Effects of cooking on mollusk shell structure and chemistry: Implications for archeology and paleoenvironmental reconstruction. J Archaeol Sci Rep. 2016;7: 14–26.
- 53. Pederson C, Mavromatis V, Dietzel M, Rollion-Bard C, Nehrke G, Jöns N, et al. Diagenesis of mollusc aragonite and the role of fluid reservoirs. Earth Planet Sci Lett. 2019;514: 130–142.
- 54. Tomašových A, Schlögl J, Biroň A, Hudáčková N, Mikuš T. Taphonomic clock and bathymetric dependence of cephalopod preservation in bathyal, sediment-starved environments. PALAIOS. 2017;32: 135–152.
- 55. Newsome SD, Yeakel JD, Wheatley PV, Tinker MT. Tools for quantifying isotopic niche space and dietary variation at the individual and population level. J Mammal. 2012;93: 329–341.
- 56. Newsome SD, Tinker MT, Monson DH, Oftedal OT, Ralls K, Staedler MM, et al. Using Stable Isotopes to Investigate Individual Diet Specialization in California Sea Otters (Enhydra lutris nereis). Ecology. 2009;90: 961–974.
- 57.
Young JZ. The Central Nervous System. In: Saunders WB, Landman NH, editors. Nautilus: The Biology and Paleobiology of a Living Fossil, Reprint with additions. Dordrecht: Springer Netherlands; 2010. pp. 215–221. https://doi.org/10.1007/978-90-481-3299-7_13
- 58. Martin JE, Vincent P, Tacail T, Khaldoune F, Jourani E, Bardet N, et al. Calcium Isotopic Evidence for Vulnerable Marine Ecosystem Structure Prior to the K/Pg Extinction. Curr Biol. 2017;27: 1641–1644.e2. pmid:28552352
- 59. Skulan J, DePaolo DJ. Calcium isotope fractionation between soft and mineralized tissues as a monitor of calcium use in vertebrates. Proc Natl Acad Sci. 1999;96: 13709–13713. pmid:10570137
- 60. Heuser A, Tütken T, Gussone N, Galer SJG. Calcium isotopes in fossil bones and teeth—Diagenetic versus biogenic origin. Geochim Cosmochim Acta. 2011;75: 3419–3433.
- 61.
Saunders WB, Ward PD. Ecology, Distribution, and Population Characteristics of Nautilus. Nautilus. Springer, Dordrecht; 2010. pp. 137–162. https://doi.org/10.1007/978-90-481-3299-7_9
- 62. Cinner JE, Zamborain-Mason J, Gurney GG, Graham NAJ, MacNeil MA, Hoey AS, et al. Meeting fisheries, ecosystem function, and biodiversity goals in a human-dominated world. 2020; 6.
- 63. Guillemot N, Léopold M, Cuif M, Chabanet P. Characterization and management of informal fisheries confronted with socio-economic changes in New Caledonia (South Pacific). Fish Res. 2009;98: 51–61.
- 64. Bevelander G. Calcification in mollusks III. Intake and deposition of Ca45 and P32 in relation to shell formation. Biol Bull. 1952;102: 9–15.
- 65. Borght OVD, Puymbroeck SV. Calcium Metabolism in a Freshwater Mollusc: Quantitative Importance of Water and Food as Supply for Calcium During Growth. Nature. 1966;210: 791. pmid:5958443
- 66. Liu Y-W, Aciego SM, Wanamaker AD. Environmental controls on the boron and strontium isotopic composition of aragonite shell material of cultured Arctica islandica. Biogeosciences. 2015;12: 3351–3368.
- 67. Hippler D, Witbaard R, van Aken HM, Buhl D, Immenhauser A. Exploring the calcium isotope signature of Arctica islandica as an environmental proxy using laboratory- and field-cultured specimens. Palaeogeogr Palaeoclimatol Palaeoecol. 2013;373: 75–87.
- 68. Kelly MW, Hofmann GE. Adaptation and the physiology of ocean acidification. Funct Ecol. 2013;27: 980–990.
- 69. Waldbusser GG, Salisbury JE. Ocean acidification in the coastal zone from an organism’s perspective: Multiple system parameters, frequency domains, and habitats. Annu Rev Mar Sci. 2014;6: 221–247. pmid:23987912
- 70. Gussone N, Langer G, Thoms S, Nehrke G, Eisenhauer A, Riebesell U, et al. Cellular calcium pathways and isotope fractionation in Emiliania huxleyi. Geology. 2006;34: 625–628.
- 71. Gussone N, Greifelt T. Incorporation of Ca isotopes in carapaxes of marine ostracods. Chem Geol. 2019;510: 130–139.
- 72. Pretet C, Samankassou E, Felis T, Reynaud S, Böhm F, Eisenhauer A, et al. Constraining calcium isotope fractionation (δ44/40Ca) in modern and fossil scleractinian coral skeleton. Chem Geol. 2013;340: 49–58.
- 73. Sime NG, De La Rocha CL, Galy A. Negligible temperature dependence of calcium isotope fractionation in 12 species of planktonic foraminifera. Earth Planet Sci Lett. 2005;232: 51–66.
- 74. Boucher-Rodoni R, Boucher G. Respiratory quotient and calcification of Nautilus macromphalus (Cephalopoda: Nautiloidea). Mar Biol. 1993;117: 629–633.
- 75.
Schipp R, Martin AW. The Excretory System of Nautilus. In: Saunders WB, Landman NH, editors. Nautilus: The Biology and Paleobiology of a Living Fossil, Reprint with additions. Dordrecht: Springer Netherlands; 2010. pp. 281–304. https://doi.org/10.1007/978-90-481-3299-7_20
- 76. Lowenstam HA, Traub W, Weiner S. Nautilus hard parts: a study of the mineral and organic constitutents. Paleobiology. 1984;10: 268–279.
- 77.
Gussone N, Dietzel M. Calcium Isotope Fractionation During Mineral Precipitation from Aqueous Solution. Calcium Stable Isotope Geochemistry. Berlin, Heidelberg: Springer Berlin Heidelberg; 2016. pp. 75–110. https://doi.org/10.1007/978-3-540-68953-9_3
- 78. Schmitt A-D, Stille P, Vennemann T. Variations of the 44Ca/40Ca ratio in seawater during the past 24 million years: evidence from δ44Ca and δ18O values of Miocene phosphates. Geochim Cosmochim Acta. 2003;67: 2607–2614.
- 79. Blättler CL, Henderson GM, Jenkyns HC. Explaining the Phanerozoic Ca isotope history of seawater. Geology. 2012;40: 843–846.
- 80. Farkaš J, Böhm F, Wallmann K, Blenkinsop J, Eisenhauer A, van Geldern R, et al. Calcium isotope record of Phanerozoic oceans: Implications for chemical evolution of seawater and its causative mechanisms. Geochim Cosmochim Acta. 2007;71: 5117–5134.
- 81. Farkaš J, Buhl D, Blenkinsop J, Veizer J. Evolution of the oceanic calcium cycle during the late Mesozoic: Evidence from δ44/40Ca of marine skeletal carbonates. Earth Planet Sci Lett. 2007;253: 96–111.
- 82. Kitch GD, Jacobson AD, Harper DT, Hurtgen MT, Sageman BB, Zachos JC. Calcium isotope composition of Morozovella over the latePaleocene–early Eocene. Geology. 2021 [cited 27 Mar 2021].
- 83. Wang J, Jacobson AD, Sageman BB, Hurtgen MT. Stable Ca and Sr isotopes support volcanically triggered biocalcification crisis during Oceanic Anoxic Event 1a. Geology. 2020 [cited 27 Mar 2021].
- 84. DePaolo DJ. Surface kinetic model for isotopic and trace element fractionation during precipitation of calcite from aqueous solutions. Geochim Cosmochim Acta. 2011;75: 1039–1056.
- 85. Mills JV, DePaolo DJ, Lammers LN. The influence of Ca:CO3 stoichiometry on Ca isotope fractionation: Implications for process-based models of calcite growth. Geochim Cosmochim Acta. 2021;298: 87–111.
- 86. Carré M, Bentaleb I, Bruguier O, Ordinola E, Barrett NT, Fontugne M. Calcification rate influence on trace element concentrations in aragonitic bivalve shells: Evidences and mechanisms. Geochim Cosmochim Acta. 2006;70: 4906–4920.
- 87. Wu HC, Dissard D, Douville E, Blamart D, Bordier L, Tribollet A, et al. Surface ocean pH variations since 1689 CE and recent ocean acidification in the tropical South Pacific. Nat Commun. 2018;9: 2543. pmid:29959313
- 88. Chen C-TA, Lui H-K, Hsieh C-H, Yanagi T, Kosugi N, Ishii M, et al. Deep oceans may acidify faster than anticipated due to global warming. Nat Clim Change. 2017;7: 890.
- 89. Qi D, Chen L, Chen B, Gao Z, Zhong W, Feely RA, et al. Increase in acidifying water in the western Arctic Ocean. Nat Clim Change. 2017;7: 195–199.
- 90. McConnaughey TA, Burdett J, Whelan JF, Paull CK. Carbon isotopes in biological carbonates: Respiration and photosynthesis. Geochim Cosmochim Acta. 1997;61: 611–622.
- 91. Zhao L, Yang F, Milano S, Han T, Walliser EO, Schöne BR. Transgenerational acclimation to seawater acidification in the Manila clam Ruditapes philippinarum: Preferential uptake of metabolic carbon. Sci Total Environ. 2018;627: 95–103. pmid:29426219
- 92. Chung M-T, Trueman CN, Godiksen JA, Holmstrup ME, Grønkjær P. Field metabolic rates of teleost fishes are recorded in otolith carbonate. Commun Biol. 2019;2: 24. pmid:30675522
- 93. Chung M-T, Trueman CN, Godiksen JA, Grønkjær P. Otolith δ13C values as a metabolic proxy: approaches and mechanical underpinnings. Mar Freshw Res. 2019 [cited 23 Oct 2019].
- 94. Romanek CS, Grossman EL, Morse JW. Carbon isotopic fractionation in synthetic aragonite and calcite: Effects of temperature and precipitation rate. Geochim Cosmochim Acta. 1992;56: 419–430.
- 95. Eide M, Olsen A, Ninnemann US, Johannessen T. A global ocean climatology of preindustrial and modern ocean δ 13 C: Climatology of Preindustrial δ 13 C. Glob Biogeochem Cycles. 2017;31: 515–534.
- 96. Eide M, Olsen A, Ninnemann US, Eldevik T. A global estimate of the full oceanic 13C Suess effect since the preindustrial. Glob Biogeochem Cycles. 2017;31: 492–514.
- 97. Auclair A-C, Lecuyer C, Bucher H, Sheppard SMF. Carbon and oxygen isotope composition of Nautilus macromphalus: a record of thermocline waters off New Caledonia. Chem Geol. 2004;207: 91–100.
- 98. Linzmeier BJ. Refining the interpretation of oxygen isotope variability in free-swimming organisms. Swiss J Palaeontol. 2019;138: 109–121.
- 99. Beirne EC, Wanamaker AD, Feindel SC. Experimental validation of environmental controls on the δ13C of Arctica islandica (ocean quahog) shell carbonate. Geochim Cosmochim Acta. 2012;84: 395–409.
- 100. Duwig C, Becquer T, Clothier BE, Vauclin M. Nitrate leaching through oxisols of the Loyalty Islands (New Caledonia) under intensified agricultural practices. Geoderma. 1998;84: 29–43.
- 101. Gaillard C, Manner HI. Yam Cultivation on the East Coast of New Caledonia: adaptation of agriculture to social and economic changes. Aust Geogr. 2010;41: 485–505.
- 102. Bouchet P, Jaffre T, Veillon J-M. Plant extinction in New Caledonia: protection of sclerophyll forests urgently needed. Biodivers Conserv. 1995;4: 415–428.
- 103. Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, et al. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature. 2005;437: 681. pmid:16193043
- 104. Pascal M, Forges BRD, Guyader HL, Simberloff D. Mining and Other Threats to the New Caledonia Biodiversity Hotspot. Conserv Biol. 2008;22: 498–499. pmid:18402591
- 105. Clark MS, Peck LS, Arivalagan J, Backeljau T, Berland S, Cardoso JCR, et al. Deciphering mollusc shell production: the roles of genetic mechanisms through to ecology, aquaculture and biomimetics. Biol Rev. 2020;95: 1812–1837. pmid:32737956
- 106. Hahn S, Rodolfo-Metalpa R, Griesshaber E, Schmahl WW, Buhl D, Hall-Spencer JM, et al. Marine bivalve shell geochemistry and ultrastructure from modern low pH environments: Environmental effect versus experimental bias. 2012 [cited 13 Sep 2018].
- 107. Beddows PA, Mallon EK. Cave Pearl Data Logger: A Flexible Arduino-Based Logging Platform for Long-Term Monitoring in Harsh Environments. Sensors. 2018;18: 530. pmid:29425185
- 108. Ullmann CV, Korte C. Diagenetic alteration in low-Mg calcite from macrofossils: a review. Geol Q. 2015;59: 3–20.
- 109. Witts JD, Newton RJ, Mills BJW, Wignall PB, Bottrell SH, Hall JLO, et al. The impact of the Cretaceous–Paleogene (K–Pg) mass extinction event on the global sulfur cycle: Evidence from Seymour Island, Antarctica. Geochim Cosmochim Acta. 2018;230: 17–45.
- 110. Benito MI, Reolid M, Viedma C. On the microstructure, growth pattern and original porosity of belemnite rostra: insights from calcitic Jurassic belemnites. J Iber Geol. 2016;42: 201–226.
- 111. Hoffmann R, Richter DK, Neuser RD, Jöns N, Linzmeier BJ, Lemanis RE, et al. Evidence for a composite organic–inorganic fabric of belemnite rostra: Implications for palaeoceanography and palaeoecology. Sediment Geol. 2016;341: 203–215.