Isotopic evidence for temperate oceans during the Cambrian Explosion

Calculation of seawater temperatures

Ninety-six spots on 13 brachiopod shells were analyzed for their oxygen isotopic composition. The δ¹⁸O_phosphate values obtained range from 9.9‰ to 17.2‰ (V-SMOW; 1σ ± 0.2‰). Oxygen isotope data vary between specimens, but also show intra-sample variations of about 3‰ up to 6‰ (samples 1599-16, 1599-38, 1599-39; see Supplementary Table 1). For calculation of paleotemperature we applied the equation of Lécuyer and co-authors⁴⁴. The major part of the Terreneuvian–Miaolingian interval is considered as an ice-free period. Assuming (1) an ice-free Cambrian ocean and therefore a δ¹⁸O_seawater value of -1.0‰^{21,22,24,27,29–31,33} or -1.4‰^17,45, and (2) considering error propagation, our reconstructed sea surface temperatures vary between 34 °C ± 12 °C and 68 °C ± 11 °C, (Fig. 1, and see Supplementary Material for additional information). In contrast, presuming an increasing δ¹⁸O_seawater over time and a global Cambrian ocean average δ¹⁸O of -6.5‰²⁵, calculated temperatures become incredible cooler, ranging from 11 °C ± 14 °C to 44 °C ± 12 °C (Fig. 1).

Diagenetic constraints

It is generally considered, that phosphate minerals are less susceptible to diagenetic alteration than carbonates. However, several studies indicate that skeletal phosphate minerals are metastable and were typically recrystallized during early diagenesis^17,46,47. Whereas no widespread diagenetic processes are known to result in an enrichment of ¹⁸O in phosphates¹⁷, more negative δ¹⁸O values are generally considered as a sign of diagenetic alteration²⁷.

In our samples, reflected light optical images already indicate recrystallization of individual shells and shell portions, which are characterized by considerably darker color and inhomogeneous appearance (Supplementary Material). SEM photographs confirm this first order identification by revealing the brachiopod shell ultrastructure in detail (Fig. 3; Supplementary Material). Dense crystalline shell material without any indication for recrystallization and alteration is characterized by δ¹⁸O_phosphate values generally more positive than 16.0‰, which thus appear to represent the most primary δ¹⁸O_seawater signature. Pores, laminae, and secondary fissures in other shell portions potentially act as pathways for fluid migration and therewith for diagenetic alteration. The visually identified recrystallized shells or portions of shells often, if not ubiquitously, yield lower δ¹⁸O_phosphate values, and are thus interpreted as most probably diagenetically altered (see Fig. 1 and Supplementary Material). Even for spots showing only initial recrystallization or partially pores, diagenetic alteration cannot be excluded with certainty. All these (probably) altered data are not included in our final discussion. The co-occurrence of both, dense crystalline and recrystallized areas in one and the same shell also explains large intra-shell variations as identified in samples 1599-16, 1599-38, or 1599-39.

Analytical constrains

Despite the obvious advantages of δ¹⁸O analyses on biogenic apatite using SIMS (e.g., analyses of very small samples or distinct shell portions), a number of sources for probable errors have to be addressed, not all of which are presently fully understood. The general chemical formula of apatite Ca₅(PO₄, CO₃)₃(CO₃, F, OH) contains three common oxygen bearing molecular groups. Whereas δ¹⁸O_phosphate analyses performed by the conventional IRMS method only isolate the PO₄³⁻ group as trisilverphosphate (Ag₃PO₄) and subsequently analyze the oxygen isotopes by high-temperature reduction^{27,29,31,37,48}, the SIMS technique indiscriminately samples oxygen from PO₄³⁻, CO₃²⁻, OH⁻, as well as residual organics^36,49. The integration of oxygen from these different sources will likely influence the SIMS-determined δ¹⁸O_phosphate values. This problem is relevant when analyzing e.g. organo-phosphatic brachiopods characterized by an alternation of carbonate-fluorapatite and organic-rich laminae. Studies on recent and fossil lingulid brachiopods have documented intra-shell δ¹⁸O_phosphate variations often exceeding 4‰ that probably represent vital fractionation effects⁵⁰. Similar intra-element δ¹⁸O_phosphate variations were detected from conodonts³⁶. Therefore, care should be taken when interpreting δ¹⁸O_phosphate values generated by SIMS. However, variations in δ¹⁸O_phosphate can be minimized by high spatial resolution SIMS analyses on the most pristine areas³⁶.

Multitude of paired SIMS and IRMS δ¹⁸O_phosphate analyses on conodonts have shown, that SIMS normally yields values 0.5–1.0‰ higher^21,33,35,36. There is still uncertainty about the systematic offset between both methods in measuring the δ¹⁸O_phosphate values in phosphate brachiopods. This unknown offset would of course bias the calculation of paleotemperatures to higher values. In this context it should be also mentioned, that coefficients in the available thermometer equations^44,51,52 were determined by IRMS (isotope ratio mass spectrometer) analyses. Whether these equations have to be adjusted for treatment of SIMS data, needs further investigation.

A probable further weakness arises from the Durango apatite standard which is commonly used to calibrate the δ¹⁸O_phosphate measurements generated by SIMS. Crystals of Durango apatite are generally assumed to be homogeneous in δ¹⁸O^53,54. A recent study, however, questions this presumption and identifies conspicuous intra-crystalline heterogeneity in δ¹⁸O in all apatite standards available⁵³. However, δ¹⁸O analyses of our samples and in house Durango apatite were performed on restricted crystal portions and δ¹⁸O_Durango values show no significant variation and a reproducibility generally better than ±0.2‰ (1σ).

Biological and paleogeographical considerations

During the early and middle Cambrian, Siberia was located in a subtropical position south of the equator⁵⁵ (Fig. 4a). Most recent simulations indicate mean sea surface temperatures of more than 35 °C for this paleogeographic region with minimum and maximum values of about 33 °C (austral winter) and 40 °C (austral summer), respectively²⁵. Similar data were modeled for Furongian to the middle Silurian equatorial to subequatorial oceans, with values varying between 30 and 35 °C⁵⁶. Comparable warm temperate ocean conditions of about 30 °C with maxima up to 37 °C (or even approaching 40 °C) are not unusual in earth history. They have also been estimated for the Triassic, Middle Jurassic, and Cretaceous times^57–59.

Average temperatures of present subequatorial ocean areas of comparable latitude to the position of Siberia in the early Cambrian vary between 24 °C (austral winter) and 35 °C (austral summer), respectively⁶⁰ (e.g., eastern Indian ocean, Java-, Banda-, Timor-, and Arafura seas; Fig. 4b,c). Assuming an ice-free Cambrian ocean and a δ¹⁸O_seawater value of -1.0‰^{21,22,24,27,29–31,33} or -1.4‰^17,45, our temperatures calculated from the most primary δ¹⁸O_phosphate values vary between 35 °C ± 12 °C and 41 °C ± 12 °C. They are thus clearly higher than modern annual subequatorial temperatures. They also often exceed the upper lethal temperature for modern marine species which is typically considered to be 38 °C with habitat-dependent fluctuations towards higher and lower values^61–64. The biological tolerance limit of 38 °C can be probably applied to Cambrian life forms, even if modern restrictions may not be strictly assumed for deep geological time.

Implications for the interpretation of the Paleozoic seawater temperature

Considering the thermal limit of 38 °C as a critical threshold, secular changes in the oxygen isotopic composition of ocean seawater are necessary to explain the presence of marine life in the Paleozoic. Based on our interpretation of the Siberian data a minimal depletion in oxygen isotopic composition of early–middle Cambrian seawater relative to today would be about -3‰. With this assumption and excluding altered and probably altered δ¹⁸O_phosphate values, calculated subtropical sea surface temperatures vary between 28 °C ± 13 °C and 32 °C ± 13 °C (Fig. 1). The minimum temperature becomes even lower (26 °C ± 13 °C) if we involve the most positive δ¹⁸O_phosphate value (17.2‰) into our calculation. These sea surface temperatures would be (1) clearly below the upper lethal limit of 38 °C of marine organisms (Fig. 1) and (2) comparable to temperatures of present subequatorial ocean areas (Fig. 4). Unexpected high temperatures calculated from the in situ measurements and bulk sample analyses of brachiopods^23,25 for the Cambrian are thus most probably an artifact of diagenetic alteration. However, the possibility of larger ¹⁸O depletions up to -6.5‰ or even -8‰²⁵ cannot be excluded completely if (1) the observed spread of data in our samples represent more than just an artifact of alteration and/or (2) other thermometer equations (e.g., Pucéat and co-authors⁵²) are applied for temperature calculation.

Oxygen isotope analyses

For oxygen isotope (δ¹⁸O) analyses, brachiopod shells were mounted centrally on two-side tape fixed on a 4.5 × 4.5 cm acrylic glass (Supplementary Material). Six grains of an in house Durango apatite standard were added and both (samples and standard) were embedded in an epoxy pellet of 2.5 cm in diameter. After hardening of about 24 hours, pellets were removed from the tape and polished to a low relief in order to minimize analytical artifacts^65,66. To facilitate navigation during SIMS analyses, a photograph image of the stub was generated using the Olympus cellSens Standard software (Supplementary Material). Prior to measurements, samples were coated with 30 nm of gold.

δ¹⁸O analyses were performed on a CAMECA ims1280 large-geometry ion microprobe at the Department of Geosciences of the Swedish Museum of Natural History (Nordsim facility). For analyses, a ¹³³Cs⁺ ion beam with an intensity of ~3 nA was critically focused and a small raster applied to homogenize the beam profile on the sample, resulting in an analyzed volume of about 10 µm width and about 2 µm depth. For calibration, two–four analyses of the Durango apatite were performed before and after six analyses of brachiopod shells. Results are reported in ‰ relative to the V-SMOW (Vienna Standard Mean Ocean Water) standard with reproducibility generally better than ± 0.2‰ (1σ). A total of 134 measurements (96 samples and 38 standard) was performed (Supplementary Material & Supplementary Table 1). Parallel to oxygen isotope measurements each analyzing spot and surrounding shell material was imaged.

Scanning electron microscopy and energy-dispersive X-ray spectroscopy

Scanning electron microscopy (SEM) was performed on the Zeiss Sigma 300 VP at the Department of Paleontology of the University of Cologne. We used the gold-coated stubs already utilized for δ¹⁸O analyses. In addition to the SEM images, energy-dispersive X-ray spectroscopy (EDS or EDXS) was applied using a X-Max^N 80 Silicon Drift Detector (Oxford Instruments) connected to the SEM. No identification of inconsistencies in element concentration could be shown by the SEM-EDS analyses (see Supplementary Material for selected spots).

All data generated or analyzed during this study are included in this published article (and its Supplementary Material).

Competing Interests

The authors declare no competing interests.