Fluctuation in redox conditions and the evolution of early Cambrian life constrained by nitrogen isotopes in the middle Yangtze Block, South China

Abstract

The Ediacaran–Cambrian (E-C) transition (∼542–517 Ma) witnessed the rapid evolution of Cambrian animals, which was accompanied by carbon cycling anomalies and a significant increase in the concentration of oxygen in Earth’s atmosphere. The mechanisms stimulating the evolution of complex eukaryotes, however, remain problematic, especially concerning the link between biological evolution and contemporaneous changes in the oceanic environment. In this study, integrated δ¹³C_carb–δ¹³C_org–δ¹⁵N compositions were analysed from the YD-4 core samples to understand redox fluctuations and nitrogen cycling of the middle Yangtze Block across the E-C transition. Two negative δ¹³C_carb excursions (N1 and N2) and a positive δ¹³C_carb excursion (P1) are identified from the studied samples and are supposedly of primary origin. Constrained by of the U-Pb age, biolithology and pattern of isotopic variation, N1, P1 and N2 are comparable to the Basal Cambrian Carbon Isotope Excursion (BACE), Zhujiaqing Carbon Isotope Excursion (ZHUCE) and Shiyantou Carbon Isotope Excursion (SHICE). We interpreted the decreased δ¹⁵N values in this study as resulting from intensified atmospheric nitrogen fixation driven by enhanced denitrification associated with expanded marine anoxia, as well as partial ammonium assimilation, while increased δ¹⁵N values suggest weakened denitrification associated with an amplified oxic water mass. The temporal coincidence of N1 and N2, with two episodes of negative δ¹⁵N excursions, and of P1, with a positive δ¹⁵N excursion, suggests that variable oceanic redox conditions and nitrogen bioavailability may have influenced the evolution of the Cambrian eukaryote-dominated community.

1. Introduction

The transition between the terminal Ediacaran and early Cambrian at ca. 542–517 Ma recorded an unprecedented biological evolution event on Earth, namely, the ‘Cambrian explosion’, resulting in the rapid diversification of metazoans during this period (Marshall, 2006; Erwin et al. 2011). The Cambrian explosion encompassed a series of episodic radiations. For example, the extinction of Ediacaran fauna occurred near the Ediacaran–Cambrian (E-C) boundary (Laflamme et al. 2013) and small shelly fauna (SSF), which are represented by the Meishucun Biota and Tommotiid, flourished in the Meishucun stage from ca. 539–521 Ma (Li et al. 2007; Zhuravlev & Wood, 2018). Afterwards, small shelly biota disappeared in the late Meishucun stage; then, Cambrian biota, represented by the Chengjiang biota of the Qiongzhusi stage, increased rapidly at ca. 521–515 Ma (Chen, 2009; Fu et al. 2019).

Investigation of the chemical environment of the ocean is an important basis for understanding the cause of the radiation of paleontological species, and among them, the reconstruction of redox conditions in the paleo-ocean is a key point. At present, there exist three hypotheses regarding the coevolutionary relationship between oxygenation events and the explosion of Cambrian life: the radiation of Cambrian life caused by a globally oxygenated atmosphere–marine system (Canfield et al. 2008; Fu et al. 2019), complete oceanic oxidation induced by Cambrian fauna and phytoplankton-induced evolution (Lenton et al. 2014; Xiao, 2012) and no causal relationship (Mills & Canfield, 2014). In past studies, redox-sensitive elements (e.g., U, V, Mo) and Fe species have been extensively used to show the redox structures in local bottom waters (Algeo & Tribovillard, 2009; Chang et al. 2018; Li et al. 2020); however, there are also limitations in applying these parameters (Algeo & Li, 2020; Liu et al. 2020). For example, the validity of Fe speciation has been questioned (Clarkson et al. 2014), especially in the context of total Fe contents <0.5% (Fan et al. 2018). As a limiting nutrient for organisms, nitrogen has remarkably different biogeochemical cycling processes and fractionation effects under different redox conditions. Since the biogeochemical process of nitrogen is sensitive to biological activities in the photic zone, the nitrogen isotope information retained in sedimentary organic matter can more effectively reveal the redox conditions of water and the position of the chemocline, as well as paleoproductivity levels (Canfield et al. 2010; Devol, 2015; Zhu et al. 2021; Wu et al. 2022). Thus, the application of nitrogen isotopes to determine the marine redox environment has distinct advantages over other common parameters, such as redox-sensitive elements and Fe species. At present, nitrogen isotope studies are increasingly being used in studies of redox conditions in South China; however, the majority of these studies focus on the lower Yangtze Block, which comprises massive shallow-water carbonate facies and basinal facies deposits (Xiaotan in Yunnan, Dingtai in Guizhou, Daotuo in Guizhou, Yinjiang in Guizhou and Yuanjia in Hunan) (Cremonese et al. 2013; Wei et al. 2017; Chen et al. 2019; Wu et al. 2022). The middle Yangtze Block sedimentary rocks that record a pattern of the nitrogen cycle within the E-C transition are still less investigated, particularly in the transitional facies; thus, nitrogen isotope studies in this region enable us to more clearly depict the redox structure of the early Cambrian Yangtze Ocean.

To reveal the biogeochemical processes related to the nitrogen cycle process and further unravel the links between environmental changes and early metazoan evolution, we conducted time series measurements of carbon isotopes of the carbonate samples (δ¹³C_carb), organic carbon isotopes (δ¹³C_org) and bulk nitrogen isotopes (δ¹⁵N) from a deep borehole in the middle Yangtze Block.

2. Geological setting

The South China Craton was located at approximately 30°N during the early Cambrian (Fig. 1a) and is composed of the Yangtze Block and the Cathaysia Block (Fig. 1b). As a result of the Neoproterozoic rifting event at approximately 820 Ma, the Yangtze Block progressively converted from a single rift basin to a continental margin basin spreading from northwest to southeast during the early Cambrian (Wang & Li, 2003); this conversion led to the development of three different depositional patterns, namely, shallow-water platform facies, transition facies and slope-basin facies (Jiang et al. 2012; Gao et al. 2016) (Fig. 1b). In terms of sedimentary sequences during the E-C transition, the shallow-water facies was dominated by carbonate deposits (e.g., the Dengying and Zhujiajing formations), and the mid- and deep-water slope basin facies were predominantly characterized by siliciclastic deposits (e.g., the Liuchapo and Laopu formations) (Och et al. 2016). During Cambrian Stages 2–3, a series of black shales were extensively formed throughout the Yangtze Block under the context of global sea level rise (e.g., Shuijingtuo and Qiongzhusi formations) (Jin et al. 2020; Chen et al. 2022).

Figure 1. (a) Early Cambrian paleogeography (∼530 Ma; adapted from Li et al. 2008); (b) paleogeographic reconstruction of the South China Craton during the earliest Cambrian, with the position of the YD-4 borehole presented in the red box (modified from Cremonese et al. 2013); (c) geological map of the study area (modified from Chen et al. 2018).

In this study, samples were obtained from the YD-4 core on the southern edge of the Huangling Uplift in the middle Yangtze Block and were formed in deep shelf palaeogeographical conditions (Chen et al. 2018; Zhang et al. 2019). Lithostratigraphically, the E-C transition in the study area includes the Dengying, Yanjiahe and Shuijingtuo formations. Among them, the Dengying Formation is mainly composed of dolomite. The Yanjiahe Formation unconformably overlies the Dengying Formation and is composed of dolomite, calcareous shale, limestone and chert. The Shuijingtuo Formation is in conformable contact with the underlying Yanjiahe Formation and mainly consists of organic-rich shale, argillaceous limestone and limestone lenses.

3. Materials and methods

In this study, 47 samples were taken from the YD-4 borehole (1283–1373 m, coordinates: 11°20′55.5″, 30°18′41.0″) that penetrates the Dengying Formation, Yanjiahe Formation and the lower part of the Shuijingtuo Formation. We measured samples for δ¹³C_carb and oxygen isotopes of carbonate (δ¹⁸O), δ¹³C_org, δ¹⁵N, as well as the carbonate weight percent, total organic carbon (TOC) and total nitrogen (TN) abundances at the Laboratory for Coastal Ocean Variation and Disaster Prediction of Guangdong Ocean University, China. Concentrations of trace elements were analysed at the Central South Mineral Resources Supervision and Testing Center of the Ministry of Natural Resources (Wuhan, China).

Sample powders (∼1 mg) were subjected to a 24-hour reaction with 100% phosphoric acid to measure the δ¹³C_carb and δ¹⁸O of carbonates using a Multicarb inlet device in-line with a 253 plus isotope ratio mass spectrometer (Spötl, 2011). The CO₂ analyte gas was separated using gas chromatography, and H₂O was eliminated using a Nafion trap before being admitted into the mass spectrometer equipped with a continuous flow interface. The international standard NBS-19 was utilized and calibrated to the Vienna Pee Dee Belemnite (V-PDB) scale. The analytical uncertainties for most samples were less than ±0.05‰ for δ¹³C_carb and δ¹⁸O based on standard analyses and ±0.1‰ based on the reproducibility of replicate analyses.

The fine-grained powders were acidified by 3 M HCl to thoroughly eliminate the carbonate component, and the percentages of calcite were then determined by utilizing these residues. The carbonate-free residues were dried overnight in an oven. The content and isotopic values of organic carbon and TN were analysed via combustion to CO₂ and N₂ using an EA Isolink series elemental analyser interfaced with a 253 plus isotope ratio mass spectrometer (IRMS). A proper amount of the residues (1∼25 mg) was transferred into a tin capsule and further introduced into a quartz combustion column at 1040 °C. Subsequently, CO₂ and N₂ entered the IRMS via He carrier gas. The N₂ and CO₂ isotopic ratios are reported in delta notation in per mil (‰) relative to atmospheric N₂ and Pee Dee Belemnite (PDB), respectively. Two carbon isotope standards (urea: δ¹³C = −28.25‰ ± 0.24‰) were inserted for each set of 10 samples, and the tested carbon isotopes of the standards generated a precision within 0.2‰. The uncertainties were generally better than 0.4‰ based on the reproducibility of replicate carbon isotopic analyses of samples. Two nitrogen isotopic standards (International standard IVA33802153: δ¹⁵N = +5.78 ± 0.1‰) were inserted for each set of 10 samples, and the tested nitrogen isotopes of the standards generated a precision within 0.2‰. Uncertainties based on the reproducibility of replicate nitrogen isotopic analyses were less than 0.3‰. The TOC and TN abundances were calculated by multiplying the percentages of carbon and nitrogen with the percentage of residue after acidification.

Trace element abundances were tested using a Thermo Scientific Element XR inductively coupled plasma mass spectrometer (ICP–MS). A proper amount of the homogenized residues (∼40 mg) was reacted with a mixture of HNO₃ + HCl + HF in a sealed Teflon cup. The Chinese national standards GSR1 (granite) and GSR3 (basalt) were employed for the purpose of uncertainty detection. The analytical precision was better than 2%.

4. Results

Our high-resolution chemostratigraphic results are presented in Fig. 2 and recorded in Table 1. The TOC abundances from the YD-4 core are typically low, with values in the range of 0.01 to 0.06% in the uppermost Dengying Formation and the lower part of the Yanjiahe Formation, followed by an increasing trend in the middle part of the Yanjiahe Formation (up to 2.54%) and then reaching a peak as high as 16.47% in the overlying Shuijingtuo Formation. Bulk carbonate δ¹³C analyses display a negative shift from 2.14‰ in the Dengying and basal Yanjiahe formations to −3.86‰ in the middle part of the Yanjiahe Formation, and then the values increase to 1.45‰ over the next 2 m. Within the basal Shuijingtuo Formation, the δ¹³C_carb values reach a nadir of ca. −5.47‰. The carbonate oxygen isotopes reveal much less short-term variability in the upper part of the Dengying Formation, with an average of −6‰, and then drop to −10‰ in the middle part of the Yanjiahe Formation followed by a 2% positive excursion in the overlying layers. The δ¹³C_org profile shows relatively stable values of approximately −29‰ in the Dengying Formation and a smooth negative shift close to −34.4‰ in the middle part of the Yanjiahe Formation. After a recovery of values to −29.8‰ at the top of the Yanjiahe Formation, another negative signal occurs at the boundary with the Shuijingntuo Formation.

Figure 2. Depth profile showing the lithostratigraphic, isotopic and elemental information from the YD-4 borehole in the Yangtze Block.

Table 1. Chemostratigraphic data from the YD-4 core

The TN abundances increase steadily up section from approximately 10 ppm in the Denying Formation to higher values, reaching 709 ppm in the Yanjiahe Formation, and then the values continuously increase to peak values of approximately 2000 ppm in the Shuijingtuo Formation. The δ¹⁵N values increase upward from high values of approximately 3.3‰ in the uppermost Dengying Formation to a low value of 0.3‰ in the middle part of the Shuijingtuo Formation; then, the values increase to 4.0‰ over the next 2 m before decreasing monotonically to −1‰ in the upper part of the Yanjiahe and the overlying Shuijingtuo Formation. The C/N values span a range of 5.4 to 141.7, with peaks corresponding to the middle part of the Yanjiahe Formation and the Shuijingtuo shale.

5. Discussion

5.a. Diagenesis

To estimate the diagenetic effect of meteoric water-derived fluids on the study areas, geochemical criteria are applied. The δ¹⁸O of carbonate is considered an effective proxy for diagenesis because high oxygen concentrations in diagenetic fluid can significantly affect δ¹⁸O (Knauth & Kennedy, 2009; Derry, 2010). Typically, δ¹⁸O values <−10‰ may present an altered δ¹³C_carb composition (e.g., Kah, 2000). Our data show that the δ¹⁸O values range from −5.2‰ to −10.8‰, with an average of −7.5‰, implying that the δ¹³C_carb composition from the YD-4 core probably preserves the primary signal. The noncoincidental observations between δ¹³C_carb and δ¹⁸O (r = 0.20, n = 31, 0.1 < p < 0.25) in the studied samples may also represent a primary cause rather than diagenesis (Fig. 3a). Indeed, a slight correlation between δ¹³C_carb and δ¹³C_org in the samples (r = 0.30, n = 31, 0.025 < p < 0.05, Fig. 3b) supports this view due to the different diagenetic effects on organic and inorganic carbon (Knoll et al. 1986). In addition, as meteoric or burial diagenesis normally raises Mn concentrations and lowers Sr concentrations, Mn/Sr values can also be considered valid proxies for evaluating diagenesis (Veizer, 1983). In carbonate samples, a Mn/Sr ratio lower than 10 is regarded as indicative of the original δ¹³C_carb composition (Kaufman & Knoll, 1995). The Mn/Sr values in this study range from 0.1 to 2.9, with an average of 1.3 (Table 1), suggesting weak diagenetic alteration. This result is also in line with the lack of a correlation between δ¹³C_carb and the Mn/Sr ratio (r = 0.24, n = 31, 0.05 < r < 0.1, Fig. 3c).

Figure 3. Crossplots of δ¹³C_carb vs. δ¹⁸O (a), δ¹³C_org vs. δ¹³C_carb (b), δ¹³C_carb vs. Mn/Sr (c), TOC vs. TN (d), δ¹⁵N vs. C_org/N_bulk (e) and δ¹³C_org vs. δ¹⁵N (f) from the YD-4 borehole. The data are presented in Table 1.

Postdepositional influence can also result in the alteration of nitrogen abundance and possible δ¹⁵N. We found that the TOC and TN abundances in this study are positively correlated (r = 0.84, n = 46, p < 0.0005, Fig. 3d), indicating a great contribution of organic molecules to TN samples. In the early diagenetic stage, preferential degradation of ¹⁴N-enriched materials (proteins and nucleic acids, etc.) could lead to a slight decrease in the C/N ratio and an increase in the isotopic value of organic nitrogen (Lehmann et al. 2002). In addition, if the samples have been influenced by thermal alteration associated with metamorphism, a selective removal of isotopically light N and C and a positive correlation between δ¹⁵N and δ¹³C_org would be expected (Busigny et al. 2003; Rivera et al. 2015). However, no clear correlations between δ¹⁵N values, C/N ratios and δ¹³C_org values are observed in this study (Fig. 3e and 3f), indicating that the δ¹⁵N composition of the YD-4 core samples was not remarkably influenced by burial fluids.

5.b. Regional stratigraphic correlation

Due to discrete fossil and chronological data, carbon isotope curves are the most reliable tool for correlations of data in the E-C transition. Although the comparisons of δ¹³C stratigraphic curves demonstrate spatial heterogeneity in the Yangtze Block (Okada et al. 2014; Chen et al. 2019), which was probably associated with the poor communication between the shallow water and the outer sea or with the missing Cambrian strata, a broad correlation has been shown in previous cases (e.g., Yuan et al. 2014; Jin et al. 2016; Wang et al. 2018). To trace carbon isotope anomalies that are closely related to the evolution of Cambrian fauna in the cores in this study and to evaluate the possible link between environmental evolution and biological events during the early Cambrian, the correlations of the stratigraphic framework in typical sections of the Yangtze Block as well as larger regions should be considered.

Many well-preserved outcrops that contain the E-C boundary have been observed in the Yangtze Block. Ishikawa et al. (2008) conducted a high-precision carbon isotope chemostratigraphic study in the Yanjiahe section, which is situated in the Three Gorges area. The general features of the carbon isotope evolution curves obtained from our samples are generally comparable with those from the Yanjiahe section (Fig. 4). There are at least two negative carbonate carbon isotope anomalies (N1 and N2) and one positive anomaly (P1) that can be identified in the study section. The first negative δ¹³C_carb excursion of ∼5‰ (N1) occurred in the lower part of the Yanjiahe Formation at the beginning of the Cambrian, and this negative shift can also be correlated with that in the contemporaneous successions in the Xiaotan section (Fig. 4), as well as the Meishucun (Brasier et al. 1990) and Laolin (Shen & Schidlowski, 2000) sections. However, the minimum of ∼−4‰ in our drill core study is moderately higher than that from other sections. This discrepancy might result from multiple reasons, including the sampling resolution and/or diagenetic effect. In addition, SSF assemblages are irreplaceable for correlations of the pretrilobitic Cambrian (Terreneuvian). Previous works have evaluated the SSF associations of the Yanjiahe Formation in several typical sections of Yanjiahe village in the Three Gorges area. The Yanjiahe Formation, in turn, contains the A. trisulcatus–P. anabarica assemblage zone, the P. antiqua assemblage zone and the A. yanjiaheensis assemblage zone (Chen, 1984; Steiner et al. 2007; Guo et al. 2014), implying that the Yanjiahe Formation is early to mid-Meishucunian in age. However, SSF associations of the Yanjiahe Formation were reported from other outcrops in the Three Gorges area, rather than from the present study core. Microscopic observations of YD-4 core samples showed only a few SSF assemblages (Cao et al., 2023), which failed to establish a continuous evolutionary association of SSF assemblages. Due to certain limitations in studying biostratigraphy based on core samples, we admit that there is uncertainty regarding the age of the lower part of the study section. Instead, we can only pay more attention from the perspectives of stratigraphic constraints and comparable carbon isotope stratigraphy. In the stratigraphic sequence of the YD-4 core, the dolorudite of the Yanjiahe Formation conformably contacts the underlying dolomite of the Dengying Formation. Thus, N1 in the YD-4 core is the first positive excursion at the base of the Cambrian. Analogously, in the Xiaotan section, a conformable contact is recognized between the Dengying Formation and the overlying Zhujiaqiong Formation, and the first negative excursion at the base of the Cambrian is believed to be the Basal Cambrian Carbon Isotope Excursion (BACE, negative δ¹³C values, Cremonese et al. 2013). Thus, we speculate that the N1 event recognized in the lower part of the Yanjiahe Formation in this study core may correspond to the BACE.

Figure 4. Stratigraphic correlation framework comparing the section in this study, the Yanjiahe section (Ishikawa et al. 2008; Okada et al. 2014), the Xiaotan section (Cremonese et al. 2013) and the Morocco section (Maloof et al. 2010).

Globally, many profiles also have the characteristic δ¹³C excursion that began in the terminal Ediacaran and reached the lowest point at the basal E-C boundary, including in Morocco (Maloof et al. 2010, see Fig. 4), the Mackenzie Mountains in NE Canada (Narbonne et al. 1994), the Anabar Platform in NE Siberia (Kaufman et al. 1996) and SW Mongolia (Brasier et al. 1996). These layers all document the first occurrence of the SSF assemblage, and thus, this negative δ¹³C_carb excursion event is also considered a global marker of the E-C boundary. Note that the tuffaceous bed in Oman provided a U–Pb age of 542 ± 0.3 Ma (Amthor et al. 2003), which is consistent with the lowest δ¹³C_carb value, further confirming the global carbon cycling response at the E-C boundary.

In the YD-4 records, the δ¹³C values show another rapid negative excursion reaching −9‰ (N2) across the boundary of the Yanjiahe-Shuijingtuo formations. The nano-SIMS U–Pb age of the base of the Shuijingtuo Formation in the Three Gorges area was estimated to be 526.4 ± 5.4 Ma (Okada et al. 2014). A previous study showed that the Shuijingtuo Formation was characterized by Hupeidiscus and Tsunyidiscus (Xue & Zhou 2006), and Zhu et al. (2003) also recognized the Atdabanian stage-type trilobites in the upper part of the Shuijingtuo Formation (Zhu et al. 2003). Trilobites first occurred at the base of the Shuijingtuo Formation (Guo et al. 2014), suggesting that the lower part of the Shuijingtuo Formation likely coincides with the latest Meishucunian age, which is comparable to the Tommotian age of the Siberian platform (Kouchinsky et al. 2012). Moreover, such a large negative isotope excursion (∼5‰ in this study) was reported in the Xiaotan, Morocco and Oman sections (Fig. 4), suggesting a global perturbation of the seawater carbon cycle. Based on the chemo- and biostratigraphic evidence and the conformable contact between the Yanjiahe and Shuijingtuo formations in the Three Gorges area, we speculate that the N2 event recognized across the Yanjiahe and Shuijingtuo Formation boundary corresponds to the Shiyantou Carbon Isotope Excursion (SHICE, negative δ¹³C values) that developed during the latest Cambrian Stage 2.

A positive excursion of +6‰ in the middle part of the Yanjiahe Formation was detected in the study core (P1). High-resolution carbon isotope evidence shows that the Zhujiaqing Carbon Isotope Excursion (ZHUCE, positive δ¹³C values) was the last positive excursion in the continuous carbon isotope perturbations between the BACE and the SHICE during the early Cambrian period (Ren et al. 2019). Combined with chemostratigraphic information of the Yanjiahe Formation, the P1 event in this study core can be correlated with the ZHUCE in the lower part of Cambrian Stage 2. This carbon isotope anomaly also exists in other sections in the Yangtze Block, such as the Xiaotan (Fig. 4), Meishucun (Brasier et al. 1990), Maidiping (Brasier et al. 1990) and Laolin (Shen & Schidlowski, 2000) sections. However, the feature of P1 in the YD-4 core is defined as a shorter duration and a lower maximum δ¹³C value (∼1.5‰) relative to other sections, which are probably due to an unconformity between the dolorudite and the overlying dark shale of the Yanjiahe Formation in the study area.

5.c. Evaluation of δ15N signals during the earliest Cambrian

Nitrogen cycle patterns in the modern ocean are important for revealing the nitrogen biogeochemical pathways preserved in sedimentary rocks (Fig. 5). The most significant source of biological nitrogen in the ocean comes from nitrogen fixation, which enzymatically converts atmospheric N₂ into biologically available nitrogen (NH₄ ⁺) through diazotrophy (mainly cyanobacteria) (Sigman et al. 2009). The most common nitrogenase enzyme for nitrogen fixation (e.g., Mo- and Fe-based enzymes) induces only a minor isotope fractionation of approximately −1‰ (ε_{product-reactan} = −2‰ to 1‰) (Stüeken et al. 2016). Direct assimilation of NO₃ ⁻ and NH₄ ⁺ is another way to capture biologically available nitrogen in the ocean, and incomplete assimilation of NH₄ ⁺ and NO₃ ⁻ can yield isotopic fractionations of ∼−4‰ to −27‰ and −5‰ to −10‰, respectively (Vo et al. 2013; Casciotti, 2009). However, this scenario occurs only under extremely high nutrient levels, for instance, eutrophication conditions at high latitudes and upwelling systems in the equatorial Pacific Ocean (Sigman et al. 2009).

Figure 5. Application of the modern nitrogen cycle to the early Cambrian marine environment. For an analysis of dominant pathways in the lower Cambrian, see the main text. Modified from Godfrey and Falkowski (2009).

The removal of fixed nitrogen from seawater is mainly determined by denitrification and anaerobic ammonium oxidation (anammox), which are both active in suboxic environments and appear today primarily in oxygen minimum zones (OMZs) and oxygen-depleted pore waters (Sigman et al. 2009; Hong et al. 2019). Denitrification can normally convert NO₃ ⁻ by anaerobic bacteria to N₂ and lead to a residual nitrate reservoir enriched in heavier ¹⁵N with fractionation values of −20 ∼ −30‰ (Brandes & Devol, 2002). The isotopic fractionation of anammox can also reach up to −25‰ (Prokopenko et al. 2006). Moreover, it was experimentally demonstrated that individual steps in nitrification can also amplify the fractionations in oxic water columns; however, net isotopic fractionation is normally not expressed via this pathway because nitrification is usually quantitatively associated with its fast rate of reaction (Lipschultz et al. 1990). Thus, the primary δ¹⁵N composition is finally determined by the equilibrium between nitrogen fixation and denitrification/anammox, and this parameter also includes reliable redox clues.

Given the buildup of δ¹³C_carb in the stratigraphic correlation framework, the BACE, ZHUCE and SHICE events have been recognized in the study area, where the BACE is coupled to a significant negative δ¹⁵N excursion (down to +0.3‰, Fig. 2). These values are distinctly lower than those from the modern ocean nitrate pool of ∼+5‰ (Sigman & Casciotti, 2001) and thus are suggested to be a strengthened nitrogen fixation signal. Environmentally controlled experiments have shown that only when seawater nitrate is consumed quantitatively at the chemocline can diazotrophy balance the nutrient structure of seawater by increasing nitrogen fixation (Sigman et al. 2009). Given that denitrification and anammox are anaerobic nitrogen cycling processes, the ¹⁵N-depleted isotopic signal associated with a slightly increasing TOC trend (up to 2.5%) might be independently explained by expanded marine anoxia in the earliest Cambrian Yangtze Sea. This scenario resembles the nitrogen isotope signal preserved in the Cretaceous Oceanic Anoxic Event (Higgins et al. 2012) and Late Devonian Hangenberg Event (Liu et al. 2016). Analogously, the SHICE across the boundary of the Yanjiahe and Shuijingtuo formations is marked by decreasing trends of δ¹³C_carb and δ¹³C_org values accompanied by relatively long-term low δ¹⁵N values at approximately −1‰. We propose that the lighter δ¹⁵N values in the SHICE would result from an insufficient nitrate pool and intensified atmospheric nitrogen fixation, as well as partial ammonium assimilation into biomass (e.g., Liu et al. 2013; Liu et al. 2020).

The ZHUCE in this study coincides with a rapidly increasing δ¹⁵N trend (up to 4.0‰), which is closer to the mean nitrogen isotope value of nitrate in modern open-ocean environments, implying that the nitrogen cycle experienced a key fluctuation during deposition of the lowermost Yanjiahe Formation. Based on the differences in net fractionation between sedimentary denitrification (∼−1 to −3‰) and water-column denitrification, reservoir box modelling emphasized that secular variation in the δ¹⁵N of sediments was dependent on the dominant locus of denitrification (Algeo et al. 2014). However, there is still controversy over the interpretation of paleoclimate and paleoenvironmental models for different nitrogen isotope distributions and their corresponding dominant locus of denitrification (Junium & Arthur, 2007; Liu et al. 2008), which may be related to differences in timescales and/or restriction of marine basins (Algeo et al. 2014). Accepting that nitrogen fixation and denitrification are considered two main end members that affect the nitrogen isotope pattern of nitrate, we propose that the ∼4‰ positive excursion in δ¹⁵N was likely a consequence of declined rates of denitrification and a deepening chemocline, thereby amplifying the oxic water mass associated with an elevated nitrate pool. However, the δ¹⁵N value increased to only 4.0‰, which is still slightly below the levels found in modern oceans, implying that the nitrate pool of surface water in the ZHUCE was lower than the current level.

5.d. Implication for early Cambrian biotic evolution

Several carbon isotope anomalies closely related to the evolution of early Cambrian life have been identified, implying temporal coupling between the prosperity/extinction of organisms and marine environmental changes (Zhu et al. 2007; Betts et al. 2018; George et al. 2021; Topper et al. 2022). For example, the diversification of Ediacaran fauna can be correlated to the Dengying Positive Carbon Isotope Excursion (DEPCE, negative δ¹³C values); the extinction of the Ediacaran fauna near the E-C boundary on a global scale is synchronous with the BACE; the rapid radiation of the SSF assemblages in Cambrian Stage 2 can be well correlated with the ZHUCE; the extinction of the SSFs in Cambrian Stage 2 corresponds to the SHICE and the initial explosion of arthropods (especially trilobites) corresponds to the Cambrian Arthropod Radiation Isotope Excursion (CARE, positive δ¹³C values) (Fig. 6).

Figure 6. Compilation of evolutionary events with δ¹³C_carb values during the early Cambrian (modified from Ren et al. 2019). The diversity data of animal genera are from Li et al. (2007) and the δ¹³C_carb curves are from Zhu et al. (2006).

The remarkable increase in dissolved oxygen levels in oceans was thought to serve as a pivotal catalyst that resulted in the innovation of primitive simple animals and their diversification (e.g., Erwin et al. 2011; Sperling et al. 2013). Indeed, the two negative δ¹⁵N excursions in this study occur synchronously in the BACE and SHICE, indicating the impact of the expansion of anoxic water masses on the living environment of the Ediacaran fauna and small shelly fauna. The BACE has a wide global response (Maloof et al. 2010; Zhu et al. 2019), and its initiation is coincident with sea level rise (Ishikawa et al. 2014). Iron speciation information provided evidence of anoxic and ferruginous environments in the Lower and Upper Yangtze areas during the E-C transition, such as the Diben section of Zhejiang, Silikou section of northern Guangxi and Longbizui and Yanwutan sections of western Hunan (Chang et al. 2010; Wang et al. 2012; Yuan et al. 2014). Given that the Rodinia breakup and Gondwana amalgamation occurred during the E-C transition, ocean circulation induced by plate movement might have led to enhanced upwelling on continental margins (Tucker, 1992; Wille et al. 2008; Ader et al. 2014; Wang et al. 2015). In this case, deep-water upwelling would have enhanced nutrient fluxes and transported ¹³C-depleted anoxic water masses to the shallow platform area. In the ZHUCE, the δ¹⁵N value (with a maximum of 4‰) is slightly smaller than that of the modern ocean, indicating that the degree of oxidation was highly associated with the deepening chemocline, which provided a favorable O₂ demand for the radiation of the small shelly fauna. The δ¹⁵N returned to 0∼−2‰ in the SHICE, which is indicative of the shallower chemocline relative to that in the BACE. The lower δ¹⁵N value in the SHICE is consistent with the largest global marine transgression during the Phanerozoic associated with strong upwelling (Goldberg et al. 2007), which would have transported the reducing deep water to the shallow-water area, thereby leading to the temporal extinction of small shelly fauna.

On the other hand, changes in the bioavailable nitrogen pool may have exerted an important influence on the regulation of eukaryotic organisms because oceanic nitrate is the preferential source of nitrogen for eukaryotic organisms (Karl et al. 2001). The variability in the oceanic nitrate pool mainly depends on the aerobic and anaerobic nitrogen cycling paths (Lehmann et al. 2002). Increased fixed nitrogen supply and episodic animal radiation have been proposed based on the coupling relationship between long-term δ¹⁵N variations and major diversifications in the metazoan group, as documented by body fossil and biomarker records (Wang et al. 2018; Wu et al. 2022). Contraction of the oceanic nitrate pool was associated with an anaerobic N cycle when the ocean became more anoxic with a shallower chemocline in the BACE and SHICE. Such nitrate limitation could have been linked to lower primary productivity and delayed radiation of eukaryotic organisms (e.g., Anbar & Knoll, 2002; Koehler et al. 2017). The aerobic N cycle and more abundant nitrate available in the surface water are shown in the ZHUCE, which could have been beneficial to the evolution from single-celled microorganisms toward a eukaryote-dominated community (e.g., Stüeken, 2013; Wang et al. 2018).

6. Conclusions

Time-series carbon and nitrogen isotopic data obtained from the YD-4 core samples across the E-C transition in the Yangtze Block present a sequence of significant disturbances, offering valuable environmental insights for the evolution of eukaryotes in the middle Yangtze Block. According to the comparison of the δ¹³C_carb curves from several representative sections in the Yangtze Block and other time-equivalent strata in other larger regions, the BACE, ZHUCE and SHICE are well constrained in the study area. Within the BACE and SHICE in the transitional facies in the middle Yangtze Block, the δ¹⁵N value displays a rapidly negative excursion (∼0‰), suggesting enhanced microbial nitrogen fixation and partial ammonium assimilation, which were likely linked to complete denitrification associated with expanded anoxic conditions. In contrast, the positive δ¹⁵N values in the ZHUCE indicate a growing nitrate pool with a deeper chemocline. Given the linkage between the carbon isotope anomaly events and the δ¹⁵N patterns, the widespread anoxic water conditions may have been related to the extinction of Cambrian-type animals, while an expansion of oxic waters and an amplified nitrate pool in the surface waters may have promoted Cambrian biodiversity.