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Calcareous nannofossil changes in the Early Oligocene linked to nutrient and atmospheric CO2
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Ruigang Ma1, Haizhang Yang2, Xiaobo Jin1, Zhao Zhao2, Gongcheng Zhang2, Chuanlian Liu1, *
Acta Oceanologica Sinica | 2020, 39(10) : 70 - 80
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Acta Oceanologica Sinica | 2020, 39(10): 70-80
• Marine Geology •
Calcareous nannofossil changes in the Early Oligocene linked to nutrient and atmospheric CO2
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Ruigang Ma1, Haizhang Yang2, Xiaobo Jin1, Zhao Zhao2, Gongcheng Zhang2, Chuanlian Liu1, *
Affiliations
  • 1 State Key Laboratory of Marine Geology, Tongji University, Shanghai 200092, China
  • 2 CNOOC Research Institute Co., Ltd., Beijing 100027, China
Published: 2020-10-25 doi: 10.1007/s13131-020-1661-6
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Rapid changes on nutrient supply and CO2 concentration that occurred in the northern South China Sea (SCS) during the Early Oligocene, provides an ideal natural laboratory, allowing us to peer into the coccolithophores’ physiology in the geological records. In this study, we established a new nannofossil assemblage index, termed as E* ratio, which is calculated by the relative abundance of eutrophic taxa and meso-oligotrophic taxa (${E^*}=\frac{e}{{e + c}}\times100$, where e is eutrophic taxa, and c is meso-oligotrophic taxa). Eutrophic taxa include small Reticulofenestra, Reticulofenestra lockeri group, Reticulofenestra bisecta group and Coccolithus pelagicus group, while meso-oligotrophic taxa include Cyclicargolithus spp. The E* ratio is well correlated with nutrient proxy during the Early Oligocene, while with different covarying patterns under the higher and lower CO2 condition. By comparing the assemblage changes to the published data, we suggest that coccolithophores may change the way they use carbon source and nutrient with the decline of CO2. Furthermore, this implies a possible initiation of the carbon concentrating mechanism.

coccolithophore  /  assemblage change  /  weathering intensity  /  carbon concentrating mechanism  /  northern South China Sea
Ruigang Ma, Haizhang Yang, Xiaobo Jin, Zhao Zhao, Gongcheng Zhang, Chuanlian Liu. Calcareous nannofossil changes in the Early Oligocene linked to nutrient and atmospheric CO2[J]. Acta Oceanologica Sinica, 2020 , 39 (10) : 70 -80 . DOI: 10.1007/s13131-020-1661-6
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1 Introduction
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Coccolithophores (marine calcifying phytoplankton) comprise up to 20% of the phytoplankton carbon pool in open ocean regions (Poulton et al., 2007). This unique phytoplankton plays an important role in the oceanic carbon cycle due to their physiological processes. The calcification (release CO2) and photosynthesis (absorb CO2) contribute to the marine carbonate-counter pump and biological pump, respectively. Studies on modern species have revealed that coccolithophores have a relatively inefficient carbon concentrating mechanism (CCM), thus can be carbon limited compared to other phytoplankton for photosynthesis under low CO2 conditions (Bach et al., 2013; Reinfelder, 2011; Riebesell, 2004; Rost et al., 2003). Besides, the growth of the coccolithophores could be influenced by many factors. For example, nitrate controls the cell growth, affecting the size of the cell, while phosphorous controls the mitosis, affecting the abundance of the cells (Müller et al., 2008). Light intensity influences the rate of the cell photosynthesis. The temperature has great limitations on the activity of enzymes, which concern with almost every physiological process within the cell (Krumhardt et al., 2017). It is widely believed that different limitations will lead to different adaptive strategies. However, existing studies tended to minimize the complexity and flexibility of the nannoplankton responses to paleoceanographic changes.
As the most successful and yet enigmatic organism in the modern ocean, the coccolithophores have the capability of adjusting their living strategy to adapt to the environmental changes (Aubry, 2007, 2009), for example, the strategy of utilizing the carbon resources. A coccolith isotopic record from Early Miocene to Pleistocene suggested that aqueous CO2 concentration of 16–19 μmol/L is the threshold of the coccolithophores’ CCM (Bolton and Stoll, 2013). During the Eocene-Oligocene Boundary, Earth’s climate has undergone a significant cooling and continental ice-sheet expanding, as revealed by the benthic δ18O (Zachos et al., 2001; Cramer et al., 2009, 2011). Atmospheric CO2 declined around 500×10–6 (volume fraction) during the Early Oligocene (Pagani et al., 2005, 2011; Zhang et al., 2013). Although there are some coccolithophores assemblage records of Oligocene (Bown et al., 2004), the study of the driving mechanisms for this physiological change are still insufficient (Plancq et al., 2013; Henderiks and Pagani, 2008; Müller et al., 2017).
The northern South China Sea (SCS) provides a relatively stable and semi-enclosed environment after its spreading since the earliest Oligocene (Li et al., 2006; Zhang et al., 2015; Jian et al., 2019; Ma et al., 2019). Yet, variations of terrestrial input caused dramatic changes in the nutrient condition during this period. Pollen analysis from ODP Site 1148 revealed that a relatively arid and cool climate was developed since 32 Ma in the nearby continent (Wu et al., 2003). In this study, we provide coccolith records and bulk sediment elemental ratios data covering 34–27 Ma from sites in the northern SCS.
2 Materials and methods
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2.1 Study sites and samples
We combined records from three sites in the northern SCS to lower the possible bias caused by the effect of redeposition on the calcareous nannofossils (Fig. 1). Sites U1501 and U1505 were retrieved during the International Ocean Discovery Program (IODP) cruise Exp. 367/368. Site U1501 (18°53′N, 115°46′E) lies on a broad basement high in the lower slope of the northern SCS at a water depth of 2 845.8 m, which is above the temporal CCD at ~3 500 m (Wang, 1999). For the first time in the region, relatively continuous sediment cores with well-preserved Early Oligocene calcareous nannofossils were recovered from this site. Sixty-seven samples were collected every 90 cm from 373.18 m to 303.95 m (CSF-A) in Hole U1501 C.
Site U1505 (18°55.0′N, 115°51.5′E) is located at a water depth of 2 916.6 m on a broad regional basement high. It was an alternate to Site U1501. Both Sites U1505 and U1501 are located on the same structural high with similar water depths and are 10.5 km apart. These two sites are believed to have similar tectonic background. Site U1505, however, have wider interval that considered as the slum zone caused by tectonic activity (Jian et al., 2019). We collected 38 samples from Hole U1505 C in the lower part of the Lower Oligocene (417.66–444.55 m), spacing varied from 40 cm to 90 cm.
Borehole LW2 (19°30′N, 115°40′E) was retrieved in the western Liwan Sub-sag, Baiyun Sag, Zhujiang (Pearl) River Mouth Basin. This industrial borehole located at around 1 800 m water depth, above the temporal CCD, which guarantees great preservation of calcareous fossils. Fifty-five samples were collected from 3 266 m to 3 841 m (total depth) from this site, spacing around 10 m.
2.2 Calcareous nannofossil
The samples were prepared following the technique of Koch and Young (2007) modified by Bordiga et al. (2015), allowing absolute quantification of nannofossil abundances per gram of sediment. The taxonomic nomenclature described in Nannotax 3 (Young et al., 2018) was followed. Each sample was prepared by weighing 0.2–0.5 g of dried bulk sediment and diluting with 100–250 mL of buffered water. Then 100–500 μL well-mixed suspension was placed on a cover slip with a high-precision pipette and dried on a hotplate at 35°C. The weight of sediment, volume of dilution and the suspension on the cover slip were adjusted according to the abundance of the nannofossil in each sample. Settled slides were examined using Zeiss Scope A1 microscope under a cross polarizer and a magnification of 1 250×. On each slide, more than 300 calcareous nannofossils were counted. For each sample, the absolute (ind./g) and relative (%) species abundances are both calculated following Bordiga et al. (2015).
Coccolith fluxes were calculated by using the following formula:
$F = X{R_{\rm{a}}}D,$
where F is the coccolith flux (ind./(mm2·ka)), X is the absolute abundance (ind./g) of total nannofossil, Ra is the accumulation rates (mm/ka) that calculated by nannofossil controlling bio-events, and D is the bulk dry-density (g/mm3) from Larsen et al. (2018).
The E* ratio as an assemblage index is for the first time developed in this study:
${E}^{*}=\frac{e}{e+c}\times 100,$
where e represents the combined relative abundance of eutrophic taxa (see Section 3.1), and c is the relative abundance of Cyclicargolithus spp. The Oligocene Nannoplankton community is featured by the great and very common appearance of the Cyclicargolithus. The Cyclicargolithus floridanus is a sub-group of the circular Reticulofenestra with a narrower central area, which is common in many Paleogene marine sections yet its ecological preference remains ambiguous. Some authors considered Cy. floridanus as a warm (Aubry, 1992) or eutrophic taxon (Aubry, 1992; Dunkley Jones et al., 2008; Auer et al., 2014; Fioroni et al., 2015), while others claimed it as an indicator of decreased nutrient supply or lower ocean productivity (Bordiga et al., 2015; Toffanin et al., 2011; Ma et al., 2019). In this study, we refer it as a non-nutrient indictive taxa, based on their cosmopolitan appearance in the ocean and through our study interval. Taxa that believed to be sensitive and indicative to nutrient condition of the sea water are as follows: C. pelagicus (Cachão and Moita, 2000; Fernando et al., 2007; Jin et al., 2016; Tangunan et al., 2018), R. lockeri group (Newsam et al., 2017; Persico and Villa, 2004; Villa et al., 2008), R. bisecta group (Persico and Villa, 2004; Villa et al., 2008) and small Reticulofenestra (Flores et al., 1995; Henderiks and Pagani, 2008; Jatiningrum and Sato, 2017). This E* ratio index is a good indicator of the community’s demand for nutrients in seawater.
2.3 Bulk sediment elemental analysis
A total of 44 samples from 379.75 m to 304.56 m (~27–34 Ma) of Site U1501 were collected for geochemical analyses. Bulk sediments were first washed with deionized distilled water, dried at 50°C for 48 h and then hand crushed in an agate mortar. Approximately 3 g of dry samples were heated to 600°C for 2 h in order to remove organic matter and interlayer water. Next, the samples were digested in a HF-HNO3 mixture, and major and trace elements were measured using ICP-AES and ICP-MS, respectively. Three certified materials (i.e., GSR-5, GSR-6, and GSD-9; provided by the Institute of Geophysical and Geochemical Exploration, China) were repeatedly analyzed as unknown samples to assess the precision and accuracy of the measurements. The external precision was usually better than 5% and concentrations obtained were in agreement with the recommended data of these reference materials. Analyses were carried out at the State Key Laboratory of Marine Geology, Tongji University.
Although many elemental proxies often have a low merit when applied to paleoenvironmental interpretations in coastal and shallow sea areas (Tribovillard et al., 2006), some elements have been shown as reliable proxies of weathering intensity, among others. In examining the climate change since 32 Ma we consider the proxies applied to weathering and erosion studies in a tectonic timescale.
Ti/Al ratio is broadly used as an eolian flux proxy, a higher Ti/Al value indicates more eolian sediment and thus a relatively arid climate. However, as we observed the samples under scanning electron microscope, we did not find any eolian sandy sediment (angular morphology of quartz) in Site U1501 during the Early Oligocene. On the other hand, titanium is concentrated in heavy minerals (e.g., ilmenite, rutile and zirconium) and in coarser silt and sand fractions (Schmitz, 1987; Shimmield and Mowbray, 1991). We thus believe that the TiO2/Al2O3 ratio in U1501 represents the paleo-stream energy in this study.
Relative changes in Al and K at this site reflect the preferential enrichment of kaolinite (low K/Al) in warm/humid period and the better survival of feldspar (high K/Al) during drier periods (Clift et al., 2014). We used phosphorus (calculated from P2O5) as a nutrient proxy because: (1) PO4 is the only source of phosphorus for phytoplankton in Earth system models (in contrast to nitrogen, which can be taken up by phytoplankton as nitrate or ammonia); (2) PO4 availability has been shown to affect coccolithophore’s calcification (Feng et al., 2017; Müller et al., 2008; Perrin et al., 2016); and (3) continental margins and marginal sediments, as the study sites of this paper, play a significant role in the cycling of phosphorus, with about 50% of total P input to the ocean deposited in marginal sediments (Filippelli, 2002).
In sea water, redox-sensitive Mn is mainly present as Mn2+, which under oxic conditions precipitates as Mn oxyhydroxide. The Mn flux across the sediment–water interface is driven by reductive dissolution of reactive Mn oxyhydroxide (Neretin et al., 2003). In bulk sediment, and a higher Mn/Al value represents a relatively oxic condition, and a lower value of Mn/Al ratio usually indicates a sub-anoxic bottom water condition. Mn oxyhydroxides are ubiquitous components of oxidized pelagic clays, and such phases are unstable under the reducing conditions normally encountered at depth in marginal and some deep-sea environments, so they are only found in the sea-floor record in slowly accumulating deposits that have remained oxygenated since the deposits formed (Calvert and Pedersen, 2007). Mn/Al ratio as proxy of bottom water redox condition and ventilation is proved to be valid (e.g., McKay et al., 2015; Wu et al., 2016).
3 Results
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3.1 Calcareous nannofossil biostratigrphy
The standard calcareous nannofossil NP-zonation (Martini, 1971) with calibrated ages for species datums (Raffi et al., 2016) were adopted in this study. Eight nannofossil bioevents ranging from Lower to Upper Oligocene are recognized in the three study sites (Table 1, Fig. 2). For Site U1501, the BO (base occurence) of common Clausicoccus subdistichus at 373.18 m (33.88 Ma) defines the closest bio-marker to Eocene-Oligocene Boundary (33.9 Ma), while the TO (top occurence) of Coccolithus formosus (32.92 Ma) at 356.99 m marks the boundary of NP21/NP22, and the TO of Reticulofenestra umbilicus (32.02 Ma) at 341.35 m the boundary of NP22/NP23. Furthermore, Zone NP 24 can be defined by the BO of Sphenolithus ciperonensis and TO of Sphenolithus distentus at 307.56 m and at 303.95 m, in the presence of Sphenolithus predistentus. The BO of S. ciperoensis (27.14 Ma) at 307.56 m approximates the Early/Late Oligocene boundary (Table 1).
Semblable but more tentative time controlls are recognized in U1505 and LW2. TO of Sphenolithus predistentus (26.93 Ma) was found at 407.45 m in U1505 and 3 285 m (total depth) in LW2. The TO of Reticulofenestra umbilicus (32.02 Ma, low latitude) was found in 424.92 m at U1505 and 3 773 m (total depth) in LW2. Because of the solubility effect, the TO of Coccolithus formosus (32.92 Ma) is difficult to be identified in U1505, and is only recognized in LW2 at the depth of 3 835 m. The Bc (base common occurence) of Clausicoccus subdistichus (33.88 Ma) (Raffi et al., 2016) in U1505 was found at the depth of 443.45 m. The TO of Sphenolithus distentus (26.84 Ma) and Sphenolithus pseudoradians (28.73 Ma) were found in LW2 at depth of 3 273 m and 3 395 m (total depth).
Age model was established based on controlling points recognized in each site with a liner interpolation in between (Fig. 2).
3.2 Nannofossil assemblages and the E* ratio
For each sample, one nannofossil species (Coccolithus pelagicus), two species group (Reticulofenestra lockeri group and Reticulofenestra bisecta group) and three genra (Cyclicargolithus, Sphenolithus and Helicosphaera) are counted. Reticulofenestra that smaller than five micrometers were all counted and calculated as the informal group small Reticulofenestra sp. Their relative abundances are plotted against sample number sequence from ~27 Ma to 34 Ma (Fig. 3). Nannofossils in U1505 were very rare in ~27–29 Ma, thus this part of assemblages is not included to avoid the invalidity in biometric analysis.
Total absolute abundances of nannofossils at IODP Sites U1501, U1505 and LW2 are of the same order of magnitude, and do not show any significant trend in the Early Oligocene. In our study interval, the size of nannofossils in the study interval does not change much, eliminating the possible effect of mass variation. Those taxa that are larger than ten micrometers, such as R. umbilicus (>14 μm), Discoaster spp., Helicosphaera spp., and Cy. abisectus were in low abundance, while small Reticulofenestra (<5 μm) are generally evenly distributed throughout our study interval (Fig. 3). Therefore, the abundance of nannofossil can to some degree be considered as the carbonate volume produced by coccolithophore. The abundance of nannofossil dramatically dropped at 32 Ma, while the nutrient proxy is at its highest value. The abundance of nannofossil soon rebounded to a higher level at about 109 g–1 in the sediment, corresponded to an increase in CaCO3 content.
Assemblage compositions show a great consistent among the three study sites. It is shown that the Cyclicargolithus (Cy. floridanus and Cy. abisectus) was the most common and dominating taxa presented in the study interval, with a relative abundance ranging from 20% to 60%. The Cyclicargolithus spp. progressively increased from ~32 Ma to 31 Ma, coinciding with the decrease in relative abundance of eutrophic taxa. This represents an essential change in nannofossil assemblage. Lower photic zone genus Discoaster spp. and Sphenolithus spp. were rare and slightly increased through the studied interval, ranging from 0% to ~10%. Other species including Pontosphaera spp., Braarudosphaera spp. and Zygbijugatus spp. were very rare and assumed to be not important to this research (Fig. 3).
Differences of the nannoplankton community among the study sites are also documented. Several bloom-like events in the group of R. lockeri are found from around 34 Ma to 31 Ma, in U1501, instead the small Reticulofenestra were rare in this interval. Reticulofenestra bisecta group were more abundant during around 32–31 Ma in Site U1505, which cannot be seen in U1501 and LW2. These differences between U1501 and the other two sites may be caused by the differences in sample preservation and the sag-specific features of the seawater.
Remarkably, the E* ratios show a great consistent trend from the three study sites. In order to compare the assemblage changes with the environmental parameters, we plotted phosphorus content in bulk sediment against the E* ratio based on Site U1501 (Fig. 4). Among the 67 samples in IODP Site U1501, 44 samples are selected to conduct the bulk elemental analysis. The E* ratio in these samples range from 13.82% to 68.75% (average=40.41%). The phosphorus content varied from 60.1×10–6 to 351.6×10–6 (average=204.4×10–6). The absolute values of both E* and phosphorus content are higher in ~32.3–33.9 Ma than that in 26.9–32.3 Ma. Intriguingly, inversed patterns of correlation between E* and bulk phosphorus content are observed. Before 32.3 Ma, the E* ratio increased with the decreasing phosphorus (r=0.51, Fig. 4b), but the p value reaches 0.067 (>0.05), indicating a weak correlation. On the contrary, E* is positively correlated to phosphorus changes after 32.3 Ma (r=0.56, p=0.001, Fig. 4a).
3.3 Bulk elemental analysis
Geochemical proxies are shown in Fig. 5. The TiO2/Al2O3 ratio decreased distinctly from 3.2 to 2.4 during the period from 32 Ma to ~30.5 Ma, reaches the lowest value of 2.37 at around 31.5 Ma (Fig. 5). The K/Al ranges from around 0.19 to 0.26 with a continuous increasing trend at the whole study interval. Two shift of K/Al ratio observed at around 32 Ma and 30.5 Ma. Meanwhile the Mn/Al ratio was exclusively at low values (no larger than 0.2) during this period. The phosphorus generally decreased with little variation at around 32 Ma. The calcium carbonates increased since 30.5 Ma, and then reached its highest value of ~30% at ~29.5 Ma. The geochemical proxies were compared with the pollen analysis by Wu et al. (2003), which indicates a shift of dominating type of the terrestrial vegetation from tropical-subtropical humid taxa into temperate montane taxa.
4 Discussion
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This study, based on the newly formed SCS basin in the Early Oligocene, aims to tackle the question of entangled controls of nutrient and CO2 on the coccolithophores. The environmental controls on the fossil records are far more complex to be captured than culturing studies. Nevertheless, with rapid changes in nutrient condition (Ma et al., 2019) and CO2 concentration (Zhang et al., 2013; Pagani et al., 2011), the northern SCS may provide an ideal natural laboratory to compare different influencing factors on the nannoplankton.
4.1 Early Oligocene paleoenvironmental changes in the northern SCS
East Asian Paleogene climates have long been regarded as controlled by the planetary wind system, which results in a climate pattern with three latitudinally distributed zones. Two humid zones located separately in the North China and South China were lithologically designated by coals and oil shales, while an arid zone in the middle was represented by red beds and evaporates (Liu et al., 2015; Quan et al., 2014). The paleo-botanical pattern in the southern China also indicates a humid climate during the Eocene-Early Oligocene (Sun and Wang, 2005). Pollen analysis revealed that a relatively cool and arid climate had developed since 32 Ma in the neighboring continent of the northern SCS (Wu et al., 2003). This humid to arid alteration is supported by our multi-proxy analysis (Fig. 5). Decreased TiO2/Al2O3 ratio revealed a lowered fluvial runoff in ~32–30.5 Ma, corresponding to the reduced chemical weathering reflected by the increase in K/Al ratio. Minimum values of Mn/Al ratio during ~32–30.5 Ma suggested the anoxic bottom water, which was probably caused weak fluvial input. Together, these suggest a climate condition of low precipitation and low chemical weathering. The reduced terrestrial input ultimately results in a lower nutrient availability to nanoplanktons in the surface water, revealed by our phosphorus content in bulk sediment (Fig. 5).
Admittedly, the variations of chemical records can also be interpreted as tectonic changes. The northern SCS was attributed to a shallow-coastal environment with the seafloor progressively spreading after the rifting since ~34 Ma (Larsen et al., 2018; Li et al., 2006). The continuous geophysical parameters and sedimentary profiles show no evidence for a large tectonic event at 32 Ma (Jian et al., 2018; Larsen et al., 2018). Therefore, we eliminate the possible effect of tectonic changes and suggest that the climate pattern was changing in response to global atmospheric forces.
The declining atmospheric CO2 was the most striking feature of climate change during this interval. The modelling studies suggest that declined CO2 may have great influence on local environment by weakening the annual precipitation, and further induce aridity in the East Asia with decreased pressure gradient from continent to ocean (Cherchi et al., 2011; Huber and Goldner, 2012; Licht et al., 2014). Some researchers stated that the decline in global atmospheric CO2 was resulted from increased chemical weathering of exposed silica (Gaillardet et al., 1999; Wan et al., 2017). However, no distinct sea-level decline was found during this interval, arguing against the prerequisite of enhanced chemical weathering (Haq and Lohmann, 1976; Li et al., 2006).
4.2 Nannofossil assembalge changes related to CO2 and nutrient supply
In our research, we test the effect of nutrient and CO2 on the coccolithophores during the Early Oligocene, northern SCS, where both the influencing factors fluctuated in a significant magnitude. Müller et al. (2017) have shown that for the modern species Emiliania huxleyi, phosphate nutrient limitation caused a decrease in both photosynthesis and calcification at all CO2 levels (ranges from 0 to 2 000 μatm, 1 atm=101.325 kPa). However, the response to phosphate is less sensitive under a nutrient-replete condition. In this case, nutrient controls the cell’s growth under oligotrophic conditions. Once nutrient became replete, there will be no more promotive effects but only constraint of CO2 concentration. This scenario was further supported by culturing studies by Bach et al. (2015).
During the Eocene-Oligocene climate transition, nannofossil assemblage study is an indispensable way to peer into the physiologic characteristics. A prolonged influence has caved in the structure of the coccolith, revealed by the decrease of the species with robust skeleton structure, suggesting that the Eocene/Oligocene event had a marked filter effect on Eocene nanoplanktons (Aubry and Bord, 2009). Instead of nutrient limitation, Henderiks and Pagani (2008) attribute the variation of coccolith size to CO2 changes. The CO2 decline makes it more difficult for larger cells to acquire enough CO2 due to their relatively lower surface area/volume ratio. In order to acquire more carbon sources from the seawater, previous studies have suggested that coccolithophore might initiate CCM in the low CO2 condition (Bach et al., 2013; Badger et al., 1998; Bolton and Stoll, 2013; Reinfelder, 2011; Riebesell, 2004; Rost et al., 2003). We tentatively adopt 19 μmol/L as the upper limit of CCM initiating threshold from culturing research (Bolton and Stoll, 2013). With reconstructed Early Oligocene tropical Pacific sea surface temperature of ~25°C (Liu et al., 2009), the estimated p(CO2) is around 650×10–6 (volume fraction) (dashed horizontal line in Fig. 6a). The CO2 concentration reached to this value in the Early Oligocene (Fig. 6). Comparing with our assemblage data, we suggest the changes in nannofossil were triggered by the carbonate chemistry condition in the ocean. With the continuous decrease in atmospheric CO2 from the Eocene, weakened diffusive efficiency had caused a great limitation of carbon sources for coccolithophores. When CO2 distinctly declined after 32 Ma, the E* ratio changed synchronously with nutrient supply. This tendency can, to some degree, indicate that coccolithophore was more sensitive to CO2 when the CCM has not progressed. When the p(CO2) declined to lower than ~650×10–6 (volume fraction) since 32 Ma, the E* ratio is more correlated with phosphorus. In this scenario, we infer that the CCM guarantees the carbon source for both calcification and photosynthesis, making nutrient the most limiting factor. Our results further imply that long-term coccolithophore species shifts as a result of oceanic changes will potentially have a more significant impact on carbon cycle feedbacks in the future, highlighting the importance of studying integrated community calcification.
5 Conclusions
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In this study, as revealed by geochemical records, a decreased weathering intensity, which reinforced the relatively arid changing event was found in the northern SCS since 32 Ma. Nannofossil assemblage index, E* ratio, is introduced. The index comprised of relative abundance between eutrophic and meso-oligotrophic taxa shows a great correlation with bulk phosphorous content with opposite covary patterns at different time intervals. Relatively weaker nutrient limitation is found under the higher CO2 condition, while nutrient limitation strengthened under the lower CO2 condition. We suggest that with CO2 concentration above the threshold value, the assemblage changes were strongly influenced by the carbon source. After the great decline of CO2, our data suggest that nutrient availability tends to be the most limiting factor of coccolithophores growth. By comparing with Bolton and Stoll (2013) threshold value (650×10–6, volume fraction), we infer that the initiation of the CCM might have strengthened the uptake of carbon sources from the seawater.
Admittedly, the lightness and salinity are two other possible influencing factors that are very difficult to reconstruct and have not been discussed in this study. Furthermore, it also lacks precise calculation to draw a conclusion only by nannofossil abundance, as the mass, volume, and growth rate of coccolith also matter to the production of biogenic carbonate. The relationship between coccolithophore and the global carbon cycle is yet to be revealed by quantitative studies in the future.
Acknowledgements
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Samples and data used in this research were provided by the International Ocean Discovery Program (IODP). We are grateful to all the shipboard scientists of IODP Expedition 367/368. Geochemical measurements were performed in the State Key Laboratory of Marine Geology, Tongji University, under the supervision of Peijun Qiao. Xiaobo Jin acknowledge the National Natural Science Foundation of China under contract No. 41806050. In the end, this study would not have been possible without the help of M-P Aubry on Paleogene calcareous nannofossil taxonomy.
Funding
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  • The National Science and Technology Major Project of the Ministry of Science and Technology of China under contract No. 2016ZX05026007-03; the National Natural Science Foundation of China under contract Nos 41876046 and 41930536.
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doi: 10.1007/s13131-020-1661-6
  • Receive Date：2020-03-18
  • Online Date：2026-03-31
  • Published：2020-10-25
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  • Received：2020-03-18
  • Accepted：2020-06-03
Funding
The National Science and Technology Major Project of the Ministry of Science and Technology of China under contract No. 2016ZX05026007-03; the National Natural Science Foundation of China under contract Nos 41876046 and 41930536.
Affiliations
    1 State Key Laboratory of Marine Geology, Tongji University, Shanghai 200092, China
    2 CNOOC Research Institute Co., Ltd., Beijing 100027, China

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表12种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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