Home Journals Articles Updates About
CN
image
收藏切换
Miocene paleoenvironmental evolution based on benthic foraminiferal assemblages in the Lufeng Sag, northern South China Sea
收藏切换
PDF
Liyuan XUE1, Xuan DING1, *, Renjie PEI2, Xiaoqiao WAN2
Acta Oceanologica Sinica | 2019, 38(3) : 124 - 137
Less
收藏切换
Acta Oceanologica Sinica | 2019, 38(3): 124-137
• Marine Geology •
Miocene paleoenvironmental evolution based on benthic foraminiferal assemblages in the Lufeng Sag, northern South China Sea
Full
Liyuan XUE1, Xuan DING1, *, Renjie PEI2, Xiaoqiao WAN2
Affiliations
  • 1 School of Ocean Sciences, China University of Geosciences, Beijing 100083, China
  • 2 School of Earth Sciences and Resources, China University of Geosciences, Beijing 100083, China
Published: 2019-03-25 doi: 10.1007/s13131-019-1405-7
Outline
收藏切换

The Miocene epoch marks the most crucial period during the Cenozoic cooling trend, characterized by the Middle Miocene Climatic Optimum (MMCO) and a series of short–lived cooling events (Miocene isotope events). To understand the paleoenvironmental evolution along the shallow water shelf in the South China Sea during the Miocene, the benthic foraminiferal assemblage and total organic carbon content (TOC) were analyzed at Hole LF 14 located in the Lufeng Sag, northern South China Sea. Three benthic foraminiferal assemblages (e.g., the Uvigerina spp. assemblage, the Cibicides spp. assemblage, and the Cibicidoides spp. assemblage), corresponding to different watermass conditions, were recognized based on Q–mode factor analysis. Early studies suggested that Hole LF14 was deposited under semienclosed bay, middle to outer shelf or even upper bathyal environment during ~18.7–4.53 Ma. The dominant Uvigerina spp. assemblage was characterized by low diversity and shallow infaunal to infaunal species, indicating a warm, low–oxygenation and eutrophic conditions since the Early Miocene to MMCO (~18.7–14.24 Ma). An abrupt sea level drop and significant faunal changes were recorded during 14.24–13.41 Ma, suggesting development of the East Antarctic Ice Sheets, which resulted in a drop of sea level and change in benthic foraminiferal assemblages along the shallow water shelf. Beyond the Uvigerina spp. assemblage, the Cibicides spp. assemblage became important during the middle–late Middle Miocene (14.24–11.54 Ma). This assemblage was dominated by epifaunal species with relative high diversity, suggesting high–energy, high–oxygenation and oligotrophic conditions with episodic supply of organic food. The dominant Cibicidoides spp. assemblage with high diversity, indicates a mesotrophic conditions with relative high–oxygen content during the Late Miocene to Pliocene (11.54–4.53 Ma). The appearance and continuous occurrence of Ammonia spp. and Pseudorotalia spp. since 10.02 Ma, may reflect the influence of the Kuroshio Current.

South China Sea  /  Lufeng Sag  /  Miocene  /  benthic foraminiferal assemblage  /  total organic carbon  /  shelf paleoenvironment
Liyuan XUE, Xuan DING, Renjie PEI, Xiaoqiao WAN. Miocene paleoenvironmental evolution based on benthic foraminiferal assemblages in the Lufeng Sag, northern South China Sea[J]. Acta Oceanologica Sinica, 2019 , 38 (3) : 124 -137 . DOI: 10.1007/s13131-019-1405-7
Full Text
Less
1 Introduction
Less
From a global climatic and evolutionary point of view, the Miocene is an important time of a series of drastic climatic shifts during the Cenozoic cooling trend (Zachos et al., 2001). As inferred from the δ18O values of planktic and benthic foraminifera, the global climate warmed again after Miocene–1 (Mi–1, ~23 Ma) and reached an optimum in the Middle Miocene (17–15 Ma), which is known as the middle Miocene climatic optimum (MMCO) (Miller et al., 1991; Wang et al., 2003; Abels et al., 2005; Smart et al., 2007; Brandano et al., 2017). During this interval, atmospheric CO2 concentrations were similar to modern levels, and a significant positive carbon isotope shift was recorded that triggered the onset of the glacial–interglacial climatic mode (Woodruff and Savin, 1991; Holbourn et al., 2004, 2007; Tripati et al., 2009; Brandano et al., 2017). There is no agreement among researchers on the mechanism resulting in this warm period. After the MMCO, Mi–3 (14.2–13.6 Ma) through Mi–6 (~9.6 Ma) events carried on the pattern of stepwise cooling, especially during Mi–3 (Wang et al., 2003). This cooling event (Mi–3) indicates the major expansion of the Antarctic ice caps, leading to their permanent existence, cooling of the bottom water, and establishment of the modern bottom water circulation (Miller et al., 1991; Wright et al., 1992; Flower and Kennett, 1995; Wang et al., 2003). This major ice sheets growth on East Antarctica further resulted in variation of global sea level and invigoration of surface ocean circulation systems, which influenced the composition of planktic and benthic foraminiferal assemblages (Thunell and Belyea, 1982; Haq et al., 1987; Flower and Kennett, 1994). Gallagher et al. (2001) noted significant changes in paleoenvironmental conditions and benthic foraminifera corresponding to global cooling and major Antarctic Ice Sheets expansion in the Gippsland Basin, southeastern Australia. A distinct change in the foraminiferal assemblage in response to expansion of the East and West Antarctic Ice Sheets is also recorded in the Port Phillip Basin of southeast Australia during the early Middle Miocene (Gourley and Gallagher, 2004).
The South China Sea (SCS) is the largest marginal sea in the West Pacific Ocean. The marginal sea is more sensitive than the open ocean in response to global changes and can often play an “enhancement” or “strengthening” role in paleoceanographic research (Wang et al., 1986). Recent studies in reconstructing paleoclimate and paleoenvironment in the SCS have been largely based on deep–sea basin records recovered by the Ocean Drilling Program (ODP) and International Ocean Discovery Program (IODP). The benthic foraminiferal δ18O and δ13C records from ODP Site 1148 (northern SCS, at a water depth of ~3 294 m) show evidence for a similar cooling trend with global climate evolution during the Late Cenozoic, including expansion of the East Antarctic Ice Sheets, Mi events, and global carbon excursions in the Miocene (Zhao et al., 2001a, b; Wang et al., 2003). Wang and Li (2009) documented the Miocene paleoenvironmental changes based on benthic foraminiferal records from the deep–sea basin of the SCS. Paleoceanographic research on the shallow marine sequence is sparse and the literature is old. Huang et al. (2012) documented changes in sedimentation and benthic foraminifera from the shallow marine sequences of the Western Foothills of Taiwan during the Miocene without interpreting the paleoenvironmental conditions. The Zhujiang (Pearl) River Mouth Basin (ZRMB) is the most developed and typical area of Neocene marine sediments in the SCS. Thus, the ZRMB is an ideal setting for studying the continental margin record of changes in the SCS during the Miocene.
Benthic foraminifera have long been recognized for their potential in marine paleoenvironmental settings, as their distribution depends on several physical, chemical, and biological factors of watermasses (Murray, 1991, 2006; den Dulk et al., 2000). Studies of dead and living benthic foraminifera have shown that they can be good indicators for oceanographic parameters, such as water depth, substrate, dissolved oxygen, and organic matter supply (Kaiho, 1994, 1999; Hohenegger, 2005; Jorissen et al., 2007). Moreover, the microhabitats and ecological preferences of benthic foraminifera have been widely used to interpret paleoenvironmental changes (Báldi, 2006; Singh et al., 2012; Deprez et al., 2015).
In this paper, Hole LF14 from the ZRMB, located on the continental shelf of the northern SCS (Fig. 1), was studied. The aims of this study are as follows: (1) to characterize the benthic foraminiferal assemblages along the hole; (2) to reconstruct the shallow–water shelf paleoenvironment in the northern SCS during the Early Miocene to the Pliocene; and (3) to improve our understanding of the paleoenvironmental changes in the continental shelf in relation to global climatic and paleoceanographic changes during the Miocene.
2 Study area
Less
2.1 Geological settings and stratigraphy
Hole LF14 studied here is located in the Lufeng Sag of the ZRMB in the northern SCS at a water depth of ~145 m (Fig. 1). The ZRMB was developed by normal faulting during the Late Mesozoic–Early Cenozoic on the passive southern Asian continental margin (Yao et al., 1994). The Paleogene syn–rifting basin was filled by lacustrine–lake deposits and finally covered unconformably by Neogene post–rifting strata (Huang et al., 2012). Six major structural units exist in the basin: Zhu I, Zhu II, and Zhu III depressions and Dongsha, Shenhu–ansha, and Panyu Low Uplifts (Gong et al., 1989; Chen, 2000). The Lufeng Sag is one of the five sags in the Zhu I Depression (Fig. 1).
After the Middle Oligocene, rapid subsidence caused a rise in local sea level and marine transgressions from south to north in the ZRMB. Seawater entered the Zhu I Depression after 21 Ma (Qin, 1996). Since then, the Zhu I Depression was considered as a restricted semienclosed bay (Qin, 1996). This restricted environment ended at 16 Ma as the Dongsha Uplift was submerged under sea level (Qin, 1996).
The Neogene sediment sequence in the ZRMB has been divided into four units formally described as formations. The lowermost unit is the Zhujiang Formation (Wang, 1985; Jiang et al., 1994). The Zhujiang Formation accumulated at delta to shelf settings in slightly deeper water, prograding to carbonate platform reef facies on the Dongsha Uplift (Wang and Li, 2009; Zeng et al., 2015). The overlying Hanjiang Formation contains mudstone and sandstone similar to the Zhujiang Formation, probably deposited also in an overall transgressive environment (Chen et al., 1994; Jiang et al., 1994). The Yuehai Formation and Wanshan Formation were interpreted as shelf deposits (Wang and Li, 2009).
2.2 Modern surface circulation
In the SCS, the modern upper water is mostly controlled by the underlying morphology of the enclosed basin and the overlying atmospheric circulation, especially the East Asian Monsoon (Wang and Li, 2009). The surface circulation pattern in the SCS exhibits a general cyclonic gyre in winter and an anticyclonic gyre in summer (Wyrtki, 1961), accompanied by a “Summer Southeast Vietnam Offshore Current” (Fang et al., 2002) (Fig. 2). This unique surface circulation pattern is the result of seasonal changes in the East Asian Monsoon. Qu (2000) suggested that the upper–layer circulation pattern is also influenced by the Kuroshio Current in its northern part.
3 Materials and methods
Less
3.1 Materials and sampling
In this paper, an interval of 1 724 m, from 676 to 2 400 m depth at Hole LF14, was studied. In total, 171 drill cutting samples were collected. The samples were taken at 10–m intervals with a span of 3–5 m.
Samples were first crushed into small fragments (about 5–10 mm in diameter), oven dried (<60°C), and weighed. Then the indurated marlstones were soaked in 10% hydrogen peroxide solution for at least 24 h, until the samples were completely disaggregated. Finally, the samples were washed over a 63 μm sieve and dried.
3.2 Data processing and analyses of benthic foraminifera
For faunal analysis, the >125 μm fraction of the residues was divided into equal aliquots with a microsplitter to obtain subsamples containing at least 100 benthic foraminiferal specimens. Generally ~150 specimens were picked from each sample. The foraminifera were identified to the species level wherever possible and counted under a binocular microscope. Taxonomic identification of benthic foraminifera was based on Hubei Institute of Geosciences (1978), Hao et al. (1980), Wang et al. (1981), Zheng (1988), Loeblich and Tappan (1994), and Holbourn et al. (2013). The benthic foraminiferal numbers per gram of dry sediment was calculated.
The diversity of fauna is generally expressed as (1) number of species (S); (2) the Shannon diversity (H, assessed diversity of the benthic foraminiferal assemblage), given by
$H = - \mathop \sum \limits_{i = 1}^S {p_i}\ln {p_i},$
where S is the number of species, pi is the proportion of the ith species, and ln is the natural logarithm; (3) Buzas and Gilson’s evenness (E, where 0 represents completely dominated assemblages and high values indicate even assemblages), given by
$E = {{\rm e}^H}/S,$
where e is the base of the natural logarithm, H is the Shannon index, and S is the number of species; and (4) dominance (D) (Levin and Gage, 1998), the percentage of the most frequent species. This analysis was based on PAST2.0 software (Hammer et al., 2001).
The percentage of planktic foraminifera (P=100%×P/(P+B)) in the total number of foraminifera (P+B) was calculated in Xue et al. (2017). The paleowater depths were quantitatively calculated based on depth ranges of benthic foraminifera using the transfer function developed by Hohenegger (2005) and later modified by Báldi and Hohenegger (2008) and Hohenegger et al. (2008). The paleowater depths of Hole LF14 fluctuated frequently between 68 and 299 m during ~18.7–4.53 Ma, suggesting a middle–outer shelf or even upper bathyal environment (Xue et al., 2018).
Q–mode factor analysis was performed to determine the benthic foraminiferal assemblages using the program developed by Klovan and Imbrie (1971). This method involves Principal Component Analysis (PCA) followed by varimax rotation. Only the genera and species whose relative abundances were >2% and presented at least in three samples were taken into the calculation.
Reconstruction of the dissolved oxygen conditions at the seafloor is based on the relative abundance of oxic species in the benthic foraminiferal assemblage. In this study, the simplified method in Báldi (2006) was followed. The oxic species were composed of “oxic indicators” defined as having >1.5 mL/L oxygen content in Kaiho (1994) or classified as “Group 5” in Kouwenhoven and van der Zwaan (2005). In this study, Cibicides spp., Cibicidoides spp., Globocassidulina subglobosa, Hanzawaia spp., Quinqueloculina spp., and Triloculina spp. were considered as the oxic species after the study by Rosoff and Corliss (1992), Kaiho(1994, 1999), Kouwenhoven and van der Zwaan (2006), and Singh et al. (2015).
The relative abundance of infaunal species was calculated to understand more about the trophic conditions (Báldi, 2006). According to Corliss (1991), the infaunal species are generally characterized by elongate, smooth, and serial shape. In this study, these species are Amphicoryna scalaris, Bolivina spp., Brizalina spp., Bulimina spp., Florilus spp., Melonis spp., Nonionella spp., Pullenia bulloides, Rectobolivina spp., Stilostomella spp., Trifarina bradyi, and Uvigerina spp. (Jorissen, 1987; de Stigter et al., 1998; den Dulk et al., 2000; Fontanier et al., 2002; Murray, 2006).
3.3 Analyses of total organic carbon content
A total of 171 samples were selected for the analyses of total organic carbon content (TOC). Samples were dried at 105°C for 2 h, and then grinded (<74 μm). Dried sediment was weighed. About 200 mg of sediment was decalcified with 10% H3PO4, and dried. The TOC was determined using a CS–580A carbon–sulfur analyzer (Eltra). The TOC measurements were taken at the Beijing Research Institute of Uranium Geology (BRIUG).
4 Biostratigraphy
Less
A detailed overview of the biostratigraphy of Hole LF14 was reported based on planktic foraminiferal events and assemblages in Xue et al. (2017). As the studied samples are drill cutting samples, only the last appearance datum (LAD) of planktic foraminiferal event was applied to avoid the influence of falling samples. The most important planktic foraminiferal events are displayed here (Table 1). Because most planktic foraminiferal events identified in the studied interval are recognized in the Miocene, the planktic foraminiferal standard global tropical/subtropical zonation of Berggren et al. (1995) is applied here. Ages in this paper are based on the Geologic Time Scale of the Neogene (Gradstein et al., 2012). The LAD of Sphaeroidinellopsis kochi is identified at 685–690 m. So the age of the top of the studied interval is 4.53 Ma. The age of the bottom (2 400 m) of the studied interval is estimated at ~18.7 Ma by using average sedimentation rate method.
5 Results
Less
5.1 Faunal and paleoenvironmental indices
Foraminifera occurred in all samples in the studied interval from 676 to 2 400 m. At the base of the interval, foraminiferal tests were filled in by sediment and some of them were recrystallized, but they exhibit a good appearance, allowing identification at the species level. For the upper part of the interval, the preservation of the foraminiferal tests was good. The species of Bolivina spp., Cibicides spp., Cibicidoides spp., Hanzawaia spp., Heterolepa spp., Lenticulina spp., Planulina spp., Rectobolivina spp., Trifarina bradyi, and Uvigerina spp. are all abundant, with the peak abundances of >20%. The distributions of quantitatively important species are shown in Fig. 3.
Benthic foraminiferal numbers per gram of dry sediment (BFN) of the studied interval vary between 11 and 426 g–1 (87 samples) with a mean value of 102 g–1 before ~14.24 Ma. However, the values are generally high (10–790 g–1, being 275 g–1 on average for 84 samples) from ~14.24 to 4.53 Ma (Fig. 4). On the contrary, percentage of planktic foraminifera (P) is generally high before ~14.24 Ma (36%–91%, being 68% on average for 82 samples) whereas the P values vary widely between ~14.24 and 4.53 Ma, from 15% to 81%, with an average of 49% (Fig. 4).
Benthic foraminiferal diversity, S, H, E and D in the studied interval of Hole LF14 show significant variability (Fig. 4). The number of species (S) varies between 14 and 35 though the studied interval with an average value of 23. The values of H are generally low (1.09–2.89, with 2.39 on average for 87 samples) with large fluctuations before ~14.24 Ma. However, the values of H are higher (2.34–3.07, being 2.75 on average for 84 samples) from ~14.24 to 4.53 Ma. The Shannon index (H) combines information on the number of species present with the evenness (E). However, fluctuations in the evenness are more noticeable. The values of H exhibit low values between 14.66 and 14.24 Ma with a minimum value of 1.8. The dominance (D) shows an opposite trend to those shown by H and E (Fig. 4).
The TOC is high (0.64%–1.14%, being 0.88% on average for 62 samples) and show a trend similar to that of P before 14.66 Ma, whereas the TOC is low (0.38%–1.08%, being 0.63% on average for 109 samples) from 14.66 to 4.53 Ma (Fig. 4).
5.2 Benthic foraminiferal assemblages and ecological interpretation
5.2.1 Benthic foraminiferal assemblages
The Q–mode factor analysis was performed for 171 samples and 39 benthic foraminiferal genera and species. On the basis of Q–mode factor analysis, three benthic foraminiferal assemblages were recognized in the studied interval (Fig. 5); these account for 84.65% of the total variance (Table 2). The benthic foraminiferal assemblage is named based on the highest Varimax score of the species (Table 3). The principal factors show higher positive loadings at different layers, thus reflecting paleoenvironmental changes. The paleoenvironmental significant of the benthic foraminiferal assemblages is interpreted based on the ecological preferences and microhabitat preferences of the benthic foraminiferal species presenting (Báldi, 2006; Székely and Filipescu, 2016). The ecological and microhabitat preferences of benthic foraminiferal species are listed in Table 4.
Uvigerina spp. assemblage
Factor 1 accounting for 62.87% of the total variance is the most significant factor in the studied interval (Table 2). Uvigerina spp. assemblage indicated by Factor 1 is dominated by Uvigerina spp. with Heterolepa spp. (mainly Heterolepa dutemplei), Lenticulina spp., and Planulina spp. as accompanying species (Table 3). The infaunal Uvigerina spp. are typical in the upper slope and outer shelf environment with high food availability and moderate oxygen depletion in fine–grained sediments (Lutze and Coulbourn, 1984; Debenay and Redois, 1997; Schmiedl and Mackensen, 1997, Schmiedl et al., 2000, 2010; Fontanier et al., 2002; Koho et al., 2008; Pérez-Asensio et al., 2012). Heterolepa spp. are epifaunal to shallow infaunal species and typical indicator of organic–rich substrate and warm water (Wang et al., 1988; Debenay and Redois, 1997). Coincidently, Lenticulina spp. are shallow infaunal species and common in high–food–flux and/or low–oxygenation environment at the seafloor (Youssef and Taha, 2013). Thus, the Uvigerina spp. assemblage probably represents a warm, low–oxygen–concentrations and eutrophic conditions.
Cibicides spp. assemblage
Factor 2 accounts for 16.97% of the total variance (Table 2). This factor is correlated with the Cibicides spp. assemblage. Cibicides spp. are the major contributor in this assemblage comprising Bolivina spp., Cibicidoides spp., and Trifarina bradyi as secondary species (Table 3). Cibicides spp. are epifaunal species living on hard substrate in high–energy conditions with strongly pulsed food supply (Gupta, 1997; Murray, 2006; Gupta and Das, 2007; Singh et al., 2012). Besides, some species of this genera (e.g., Cibicides wuellerstorfi) have also been considered as an indicator of a high seasonal food supply in oligotrophic environment (Loubere and Fariduddin, 1999). Bolivina genera, such as Bolivina robusta and Bolivina dilatata, are shallow to deep infaunal species, which usually occur in a wide range of mesotrophic to eutrophic environments, and are especially resistant to low–oxygen conditions (Melki et al., 2010; Sgarrella et al., 2012). Kuhnt et al. (1999) earlier noted that the Bolivina spp. could be used as indicators of enhanced C–flux rates in the SCS, as pointed out by Hess and Kuhnt (1996). As a consequence, the Cibicides spp. assemblage is indicative of a high–energy, high–oxygen–content and oligotrophic environment with episodic organic matter input.
Cibicidoides spp. assemblage
Factor 3 correlated with the Cibicidoides spp. assemblage accounts for 4.81% of the total variance (Table 2). Cibicidoides spp. are important in this assemblage. Some of the associated species of this assemblage are Ammonia spp., Bolivina spp., Hanzawaia spp., Planulina spp., Pseudorotalia spp., Rectobolivina spp., and Siphonina spp. (Table 3). Cibicidoides spp. are usually described as epifaunal to infaunal in oligo–mesotrophic environments with well–oxygenated and unstable conditions (Kaiho, 1994; Murray, 2006; Melki et al., 2009; Takata et al., 2010; Sgarrella et al., 2012), although some authors argue that this genera/species can tolerate low oxygen concentrations (Rathburn and Corliss, 1994; Szarek et al., 2007). The presence of Hanzawaia spp. with a clinging mode life indicates a high–energy, food–limited environment (Kitazato, 1994; Schönfeld, 1997; Murray, 2006), for example, on the Sunda Shelf in the southern SCS (Szarek et al., 2007). Pseudorotalia spp. have been reported to be typical warm member of the Indo–Pacific shelf assemblage in tropical water characterized by coarse substrate and being less sensitive to water depth (Murray, 1991; Gallagher et al., 2009; Minhat et al., 2016). Ammonia spp., such as Ammonia beccarii, is a shallow infaunal and low salinity tolerant species occurring in the inner–middle shelf. This species is quite often found in association with mesotrophic and hypoxic environments (Murray, 1991, 2006; Báldi, 2006; Pérez-Asensio et al., 2012; Minhat et al., 2016). In the Zhujiang (Pearl) River Estuary (water depth less than 10 m), the relative abundance of this species is particularly high as it can tolerate a wide range of salinity (Li et al., 2011). Siphonina spp. are epifaunal to shallow infaunal species and are related to oligotrophic and oxic environments (Jones, 1994; Szarek et al., 2007). It is thus inferred that this faunal assemblage broadly indicates a relatively high–oxygen–content and mesotrophic environment.
5.2.2 Changes in benthic foraminiferal assemblages
During the Early Miocene–early Middle Miocene (~18.7–14.24 Ma), the high–food–exploiting Uvigerina spp. assemblage develops significantly along with higher relative abundances of Uvigerina spp., Heterolepa dutemplei, and Lenticulina spp. (Figs 3 and 5). Moreover, the Cibicidoides spp. assemblage also shows relatively high loadings during 16–14.24 Ma. The typical low–food–exploiting Cibicides spp. assemblage becomes important and remained dominant during the middle–late Middle Miocene (14.24–11.54 Ma) (Fig. 5). The Cibicidoides spp. assemblage becomes dominant during the Late Miocene to Pliocene (11.54–4.53 Ma) (Fig. 5). The relative abundances of Rectobolivina spp. and Siphonina spp. exhibit a rapid rise at 11.54 Ma, meanwhile Cibicides spp. decrease significantly (Fig. 3). Besides, the relative abundances of Ammonia spp. and Pseudorotalia spp. increase rapidly after 10.02 Ma and appear continuously during the Late Miocene and Pliocene interval (Fig. 3).
6 Discussion
Less
Benthic foraminiferal assemblage, species diversity, and TOC have been widely applied to paleoenvironmental reconstruction. Shifts in these factors indicate changing environmental conditions such as food supply and oxygenation, which may be linked to water depth (Gebhardt et al., 2004; Gupta and Kawahata, 2006; Jorissen et al., 2007). There is a causal relationship between changes in the trophic conditions and variations in the diversity and microhabitat preferences (Pérez-Asensio et al., 2012). Generally, oligotrophic environments are dominated by epifaunal species and have rather low diversity; mesotrophic environments show highest diversity and all microhabitats are represented; and finally, eutrophic environments are characterized by low diversity and dominance of (deep) infaunal species (Jorissen et al., 1995; Pérez-Asensio et al., 2012). Therefore, benthic foraminifera provide a useful tool for understanding the environmental variations in response to various paleoclimatic and paleoceanographic changes.
According to the three principal factors, diversity indices and percentage of planktic foraminifera (P), the studied interval was divided into three stages from the bottom up (Fig. 5). We compare the data of Hole LF14 with the records of δ18O and δ13C from ODP Site 1148 (Wang et al., 2003), to discuss the shallow–water environment changes in the SCS during the Miocene. The depositional environment related to water depth has been distinguished after Katz et al. (2003): inner shelf (0–50 m), middle shelf (50–100 m), and outer shelf (100–200 m).
6.1 Eutrophic conditions in the Early Miocene to early Middle Miocene, 2 400–1 550 m (~18.7–14.24 Ma)
According to the variations of the species diversity indices, paleowater depths, and loadings of the Cibicidoides spp. assemblage, the Stage 1 can be subdivided into two parts: the Early Miocene (~18.7–17.54 Ma) and the MMCO (17.54–14.24 Ma).
6.1.1 Early Miocene (~18.7–17.54 Ma)
This period is dominated by the Uvigerina spp. assemblage, suggesting warm, low–oxygen–concentrations and eutrophic conditions during ~18.7–17.54 Ma. This is supported by the relative high values of TOC (0.64%–1.08%, being 0.81% on average) and low percentage of oxic species (Figs 4 and 6).
Species diversity patterns (S, H and E) are generally low and characterized by significant fluctuation during this period (Fig. 4). In modern benthic foraminiferal assemblages, decreased diversity is associated with unstable and eutrophic environments (Sanders, 1969; Bollmann et al., 1993; Wade and Bown, 2006). Further, Jorissen et al. (1995) suggested that a eutrophic environment is commonly characterized by low diversity and dominance of (deep) infaunal species.
The paleowater depths vary between 122 and 299 m, being 173 m on average (Fig. 6), which should indicate outer shelf or even upper bathyal environment (Xue et al., 2018). Li et al. (2004a) suggested that the percentage of planktic foraminifera in the modern shelf (water depth of 100–200 m) of the northern SCS varies between 49% and 98%, being 81% on average. The percentage of planktic foraminifera (63%) of Hole LF14 (Fig. 4) is coincident with the result of paleowater depths. Qin (1996) also suggested that this period is characterized by a high sea level in the ZRMB.
However, the Zhu I Depression was considered as a restricted semienclosed bay (Qin, 1996), rather than an outer shelf environment indicated by paleowater depths of Hole LF14 during this period, which may result in poor water exchange in the Lufeng Sag. In an environment with high organic input, the remineralization of organic matter decreases the oxygen concentrations on the seafloor (Jorissen et al., 1995; Mojtahid et al., 2009). Thus, the study area is interpreted as a warm, low–oxygenation and eutrophic semiclosed bay during ~18.7–17.54 Ma.
6.1.2 Middle Miocene climatic optimum (17.54–14.24 Ma)
Uvigerina spp. assemblage is still dominant during 17.54–14.24 Ma, accompanied by the distinct development of the Cibicidoides spp. assemblage, indicating warm, relatively low–oxygenation and eutrophic conditions. A gradual increase in oxic species suggests increasing seafloor oxygenation, especially after 16 Ma (Fig. 6). Warm water benthic indicators, such as Heterolepa spp., show high relative abundance in this part suggesting that the oceanic conditions were warm during 17.54–14.24 Ma. At Hole BY7–1–1, the warm water species Sphenolithus and Discoaster show high values (e.g., 25%–35% and 16%–18%, respectively), implying that a warm surface water during 17.54–14.24 Ma (Xu, 1996). Zhao et al. (2001a) also noted a warm bottom water condition in the SCS based on the light values of δ18O of ODP Site 1148 during this period. The above analysis allows us to infer that the northern SCS is characterized by a warm water condition during 17.54–14.24 Ma.
The paleowater depths of Hole LF14 are high in the stage. The paleowater depths vary between 115 and 252 m, being 163 m on average (Fig. 6) (Xue et al., 2018), which is further supported by the high percentage of planktic foraminifera (71%) (Fig. 4). A high sea level, based on the abundances of planktic foraminifera and calcareous nannofossils, has been reported in the ZRMB during 17.54–14.24 Ma (Qin, 1996; Xu, 1996). The Dongsha Uplift is characterized by high subsidence rate during this period (Xie et al., 2014). This may provide an explanation for the submersion of the Dongsha Uplift at 16 Ma (Qin, 1996), to result in open shelf environment.
According to Jorissen et al. (1995), the low species diversity patterns (S, H and E) also suggest eutrophic conditions during 17.54–14.24 Ma. The TOC shows high values during 17.54–14.66 Ma, indicating a high sea surface productivity and high organic flux to the seafloor (Fig. 4). Based on the high values of planktic foraminiferal abundance, δ13C, percentages of Uvigerina and Bulimina (U+B), and ratios of infaunal/epifaunal (I/E), Dong and Wan (1996) suggested that the ZRMB is characterized by a high sea surface productivity during 17.54–14.24 Ma. This is a period of MMCO, characterized by low mean δ18O, high mean δ13C, and burial of organically preferred 12C–rich carbon in the world oceans (Vincent et al., 1985; Zachos et al., 2001; Singh et al., 2012). Wang et al. (2003) have identified the MMCO in the SCS based on the decrease of benthic foraminiferal δ18O of ODP Site 1148 during 17.8–13.2 Ma (Fig. 6). Besides, the carbon isotope records of the world oceans are characterized by the high δ13C values of planktic and benthic foraminifera between 17.5 and 13.5 Ma, which is also known as the Monterey Carbon Isotope Excursion (Vincent and Berger, 1985; Banerjee et al., 2017). Wang et al. (2003) suggested that the Monterey excursion is also prominently displayed at ODP Site 1148, reflecting accumulation of diatom–rich deposits in the Pacific Rim. The decline of species diversity patterns (S, H and E), TOC and P between ~14.66 and 14.24 Ma may be explained by the drastic fluctuation in paleowater depths (Fig. 6), possibly caused by a short–lived tectonic uplift in the Lufeng Sag and Dongsha Uplift (Xie et al., 2014; Xue et al., 2018). It is inferred that rising sea level results in open sea environment and gradually increases seafloor oxygenation, however, the high primary productivity and organic carbon storage make a eutrophic outer shelf or even upper bathyal environment. Consequently, the dominance of the Uvigerina spp. assemblage and high TOC show a good correlation with the MMCO.
6.2 Oligotrophic conditions in the middle to late Middle Miocene, 1 550–1 240 m (14.24–11.54 Ma)
The Cibicides spp. assemblage becomes important, suggesting a high–energy, high–oxygenation, and oligotrophic environment with pulsed organic matter input during the middle–late Middle Miocene (Fig. 5). The high percentage of oxic species of Hole LF14 also indicates a high seafloor oxygenation (Fig. 6). The paleowater depths fluctuate between 94 and 198 m, being 149 m on average, suggesting a middle to outer shelf environment (Fig. 6) (Xue et al., 2018). The shift in lithology from mud to silt–mud alternating layer at ~14.24 Ma is accompanied by decreasing paleowater depths (Figs 4 and 6). This suggests frequent alternations of dark and light sediments upward may be caused by frequent fluctuations of paleowater depths.
The TOC values were high from 13.80 to 13.41 Ma (Fig. 4). A high TOC, caused by prevailing of upwelling in the Pacific Rim due to global cooling, has also been reported from Hole PY33–1–1 during 14.24–13.41 Ma (Wan et al., 1996). Besides, the relative abundances of Uvigerina spp. and Heterolepa dutemplei show significant decreases at Hole LF14 during 14.24–13.41 Ma (Fig. 3). A similar faunal change is also observed from shallow marine sequences of the Western Foothills in Taiwan (Huang et al., 2012). Huang et al. (2012) suggested that the decline of benthic foraminifera (e.g., Heterolepa praecincta and Uvigerina nitidula) during 14.5–12.9 Ma and extinction of the endemic benthic species (e.g., Textularia kansaiensis, Textularia akaminei, and Bigenerina shihtiensis) could partly be attributed to sea level drop due to the expansion of the Antarctic Ice Sheets. Our records are consistent with the study of Huang et al. (2012). However, we assume that this faunal change is caused by the sea level drop and decreased food supply and the improved seafloor oxygenation in response to the expansion of the Antarctic Ice Sheets (Fig. 6). A noticeable shoaling in paleowater depths and declining P were recorded at Hole LF14 from 14.24 to 13.41 Ma (Fig. 6). At Hole BY7–1–1, this is a period of regression, characterized by low sea level and cool water condition (Xu, 1996). However, the low tectonic subsidence rate (~50 m/Ma) indicates that tectonic subsidence should not be the main factor resulting in this sea level drop (Xue et al., 2018). Qin (1996) assumed that this remarkable sea level drop in the ZRMB resulted from global cooling and expansion of the Antarctic Ice Sheets. At ODP Site 1148, the Middle Miocene δ18O level increases during 14.5–13.6 Ma with a 0.9‰ enrichment (Zhao et al., 2001a). The variation in the amplitude of the Cenozoic deep sea δ18O signal largely reflects changes in continental ice volume and temperature (Miller et al., 1991; Zachos et al., 2001). Flower and Kennett (1994) suggested that Mi–3 indicates major ice sheets growth on East Antarctica, resulting in high–amplitude variations of global sea level, invigoration of surface ocean circulation systems, and changes in planktic and benthic foraminiferal assemblages. Therefore, the changes in paleowater depths, benthic species and TOC at Hole LF14 in the period correspond with the key time of global cooling (Mi–3) and changes in global sea level and benthic foraminiferal assemblages.
6.3 Mesotrophic conditions in the Late Miocene to Pliocene, 1 240–676 m (11.54–4.53 Ma)
The Cibicidoides spp. assemblage, suggesting a high oxygenation and mesotrophic environment, is important during 11.54–4.53 Ma (Fig. 5). The species diversity (S, H and E) is the highest throughout the hole. Both epifaunal and (shallow) infaunal species, e.g., Bolivina spp., Cibicidoides spp., and Hanzawaia spp., are important in the Cibicidoides spp. assemblage, indicating a mesotrophic environment during 11.54–4.53 Ma (Jorissen et al., 1995; Sgarrella et al., 2012; Pérez-Asensio et al., 2012).
The percentage of oxic species decreases slightly, but remains high during this period (Fig. 6). The paleowater depths are shallow and relatively stable, varying between 68 and 151 m, being 116 m on average (Fig. 6) (Xue et al., 2018). The global climate cooling trend continues, but show no large fluctuations during the Late Miocene to Pliocene (11.54–4.53 Ma), as inferred by the mean δ18O values (Zachos et al., 2001; Wang et al., 2003). The TOC is low during 11.54–4.53 Ma, especially samples between 1 030 m and 880 m (0.38%–0.71%, being 0.47% on average) (Fig. 4). Benthic foraminiferal abundance interferes with oxygen and food levels at the seafloor affecting the P (van Hinsbergen et al., 2005; Milker, 2010). The values of P (53%–81%, being 72% on average) between 1 030 m and 880 m are relatively high compared to the paleowater depths (96–144 m, being 118 m on average). This may be explained by the low benthic foraminifera number due to lack of organic food. Therefore, the study area is middle–outer shelf environment characterized by relative high oxygenation and mesotrophic conditions during the Late Miocene to Pliocene.
The rapid increase of Rectobolivina spp. and Siphonina spp. at 11.54 Ma may be related to the increased food supply and slightly decreased oxygenation (Figs 3 and 6). The Cibicidoides spp. assemblage is also highlighted by the appearance and continuous occurrence of Ammonia spp. and Pseudorotalia spp. since 10.02 Ma (Fig. 3). Huang et al. (2012) documented that the benthic foraminifera of euryhaline species (e.g., Ammonia cf. japonica and Ammonia altispira) appear first, then the normal marine species (e.g., Asterorotalia yabei and Pseudorotalia tikutoensis) appear in the shallow water sequence of the Western Foothills of Taiwan since the transgression started at 10.2 Ma (Fig. 6). However, Ammonia spp. and Pseudorotalia spp. appear nearly at the same time at Hole LF14 (Fig. 3), which is located in the relatively deep environment in the Lufeng Sag. Huang et al. (2012) also suggested that the appearance of the new fauna at 10.2 Ma may represent an initiation of the modern Kuroshio Current by an intensification of the Western Boundary Current of the North Pacific. Tectonically, the Indo–Pacific seaway begins to close as a result of the subduction–collision between the Australia continent and the Indonesia Banda Arc in the Late Miocene (12–8 Ma) (Kennett et al., 1985; Huang, 1989; Li and Jian, 2001; Kuhnt et al., 2004; Li et al., 2004b; Kamikuri et al., 2009; Hall, 2012; Kamikuri and Moore, 2017). This event may account for an initiation of modern Kuroshio Current by an intensification of the Western Boundary Current of the North Pacific, leading to a distinct faunal change in the continental shelf of Taiwan (Huang et al., 2012). Therefore, the continuous occurrence of Ammonia spp. and Pseudorotalia spp. species may suggest that the study area is influenced by the Kuroshio Current since ~10.02 Ma.
7 Conclusions
Less
Benthic foraminifera from 171 samples of Hole LF14 have been studied. Three distinct benthic assemblages are defined by Q–mode factor analysis. These assemblages, together with their corresponding ecological and microhabitat preferences, P, diversity indices and TOC are used in reconstructing the Lufeng Sag paleoenvironmental changes through the Miocene to Pliocene.
The dominance of the Uvigerina spp. assemblage and low diversity suggest warm, low–oxygen concentrations and eutrophic conditions during ~18.7–14.24 Ma. High values of TOC suggests an increased food flux to the seafloor. The low oxygen concentrations may be associated with a semiclosed bay with poor water exchanges and the MMCO, causing high food flux to the seafloor. High diversity and dominance of the Cibicides spp. assemblage suggest high–energy, high–oxygenation and oligotrophic conditions with episodic terrestrial matter input during the middle–late Middle Miocene. The sea level drop and changes in benthic foraminifera (e.g., Uvigerina spp., Heterolepa dutemplei, and Cibicides spp.) reflect a global cooling and major expansion of the Antarctic ice sheets. The Cibicidoides spp. assemblage, indicating relative high–oxygen content and mesotrophic conditions, becomes important during the Late Miocene–Pliocene. The appearance and continuous occurrence of Ammonia spp. and Pseudorotalia spp. after 10.02 Ma is possibly caused by the intensified Western Boundary Current of the North Pacific.
Acknowledgements
Less
We thank the China National Offshore Oil Corporation for providing samples used in this study.
Funding
Less
  • The National Natural Science Foundation of China under contract No. 91328201.
References
Less
Abels H A, Hilgen F J, Krijgsman W, et al. 2005. Long-period orbital control on middle Miocene global cooling: integrated stratigraphy and astronomical tuning of the Blue Clay Formation on Malta. Paleoceanography, 20(4): PA4012
Báldi K. 2006. Paleoceanography and climate of the Badenian (Middle Miocene, 16.4–13.0 Ma) in the Central Paratethys based on foraminifera and stable isotope (δ18O and δ13C) evidence. International Journal of Earth Sciences, 95(1): 119–142, doi: 10.1007/s00531-005-0019-9
Báldi K, Hohenegger J. 2008. Paleoecology of benthic foraminifera of the Baden-Sooss section (Badenian, Middle Miocene, Vienna Basin, Austria). Geologica Carpathica, 59: 411–424
Banerjee B, Ahmad S M, Raza W, et al. 2017. Paleoceanographic changes in the Northeast Indian Ocean during middle Miocene inferred from carbon and oxygen isotopes of foraminiferal fossil shells. Palaeogeography, Palaeoclimatology, Palaeoecology, 466: 166–173, doi: 10.1016/j.palaeo.2016.11.021
Berggren W A, Kent D V, Swisher C C, et al. 1995. A revised Cenozoic geochronology and chronostratigraphy. In: Berggren W A, Kent D V, Aubry M P, and Hardenbol J eds. Geochronology Time Scales and Global Stratigraphic Correlation: an Unified Temporal Framework for Historical Geology. Society of Economic Paleontologists and Mineralogists Special Publication, 54: 129–212
Bollmann J, Hilbrecht H, Thierstein H R. 1993. Evenness and species-richness in modern coccolith and foraminifera assemblages. International Nannoplankton Association Newsletter 15/2, 55
Brandano M, Cornacchia I, Raffi I, et al. 2017. The Monterey event within the central Mediterranean area: the shallow-water record. Sedimentology, 64(1): 286–310, doi: 10.1111/sed.2017.64.issue-1
Chen Changmin. 2000. Petroleum geology and conditions for hydrocarbon accumulation in the eartern Pearl River Mouth Basin. China Offshore Oil Gs (Geol) (in Chinese), 14(2): 73–83
Chen Jishu, Xu Shice, Sang Jinyu. 1994. The depositional characteristics and oil potential of paleo Pearl river delta systems in the Pearl river mouth basin, South China Sea. Tectonophysics, 235(1–2): 1–11, doi: 10.1016/0040-1951(94)90013-2
Corliss B H. 1991. Morphology and microhabitat preferences of benthic foraminifera from the northwest Atlantic Ocean. Marine Micropaleontology, 17(3–4): 195–236, doi: 10.1016/0377-8398(91)90014-W
de Stigter H C, Jorissen F J, van der Zwaan G J. 1998. Bathymetric distribution and microhabitat partitioning of live (Rose Bengal stained) benthic foraminifera along a shelf to bathyal transect in the southern Adriatic Sea. Journal of Foraminiferal Research, 28: 40–65
Debenay J P, Redois F. 1997. Distribution of the twenty seven dominant species of shelf benthic foraminifers on the continental shelf, north of Dakar (Senegal). Marine Micropaleontology, 29(3–4): 237–255, doi: 10.1016/S0377-8398(96)00034-5
den Dulk M, Reichart G J, van Heyst S, et al. 2000. Benthic foraminifera as proxies of organic matter flux and bottom water oxygenation? A case history from the northern Arabian Sea. Palaeogeography, Palaeoclimatology, Palaeoecology, 161(3–4): 337–359, doi: 10.1016/S0031-0182(00)00074-2
Deprez A, Tesseur S, Stassen P, et al. 2015. Early Eocene environmental development in the northern Peri-Tethys (Aktulagay, Kazakhstan) based on benthic foraminiferal assemblages and stable isotopes (O, C). Marine Micropaleontology, 115: 59–71, doi: 10.1016/j.marmicro.2014.11.003
Dong Junshe, Wan Xiaoqiao. 1996. A preliminary study of the Neogene Paleoproductivity in Pearl River Mouth Basin. In: Research on Micropalaeontology and Paleoceanography in the Pearl River Mouth Basin, South China Sea (in Chinese). Wuhan: China University of Geology Press, 129–136
Douglas R G. 1981. Paleoecology of continental margin basins: a modern case history from the borderland of southern California. In: Douglas R G, Colburn I P, Gorsline D S, et al. eds. Depositional Systems of Active Continental Margin Basins. Pacific Section, Society of Economic Paleontologists and Mineralogists Short Course Notes, 121–156
Ernst S R, Guasti E, Dupuis C, et al. 2006. Environmental perturbation in the southern Tethys across the Paleocene/Eocene boundary (Dababiya, Egypt): foraminiferal and clay mineral records. Marine Micropaleontology, 60(1): 89–111, doi: 10.1016/j.marmicro.2006.03.002
Fang Guohong, Fang wending, Fang Yue, et al. 1998. A survey of studies on the South China Sea upper ocean circulation. Acta Oceanographica Taiwanica, 37(1): 1–16
Fang Wendong, Fang Guohong, Shi Ping, et al. 2002. Seasonal structures of upper layer circulation in the southern South China Sea from in situ observations. Journal of Geophysical Research, 107(C11): 3202, doi: 10.1029/2002JC001343
Fiorini F. 2015. Recent benthic foraminifera from the Caribbean continental slope and shelf off west of Colombia. Journal of South American Earth Sciences, 60: 117–128, doi: 10.1016/j.jsames.2015.03.003
Flower B P, Kennett J P. 1994. The middle Miocene climatic transition: East Antarctic ice sheet development, deep ocean circulation and global carbon cycling. Palaeogeography, Palaeoclimatology, Palaeoecology, 108(3–4): 537–555, doi: 10.1016/0031-0182(94)90251-8
Flower B P, Kennett J P. 1995. Middle Miocene deepwater paleoceanography in the southwest Pacific: relations with East Antarctic Ice Sheet development. Paleoceanography, 10(6): 1095–1112, doi: 10.1029/95PA02022
Fontanier C, Jorissen F J, Chaillou G, et al. 2003. Seasonal and interannual variability of benthic foraminiferal faunas at 550 m depth in the Bay of Biscay. Deep–Sea Research Part I: Oceanographic Research Papers, 50(4): 457–494, doi: 10.1016/S0967-0637(02)00167-X
Fontanier C, Jorissen F J, Licari L, et al. 2002. Live benthic foraminiferal faunas from the Bay of Biscay: faunal density, composition, and microhabitats. Deep–Sea Research Part I: Oceanographic Research Papers, 49(4): 751–785, doi: 10.1016/S0967-0637(01)00078-4
Gallagher S J, Smith A J, Jonasson K, et al. 2001. The Miocene palaeoenvironmental and palaeoceanographic evolution of the Gippsland Basin, Southeast Australia: a record of Southern Ocean change. Palaeogeography, Palaeoclimatology, Palaeoecology, 172(1–2): 53–80, doi: 10.1016/S0031-0182(01)00271-1
Gallagher S J, Wallace M W, Li C L, et al. 2009. Neogene history of the West Pacific Warm Pool, Kuroshio and Leeuwin currents. Paleoceanography, 24(1): PA1206
Gebhardt H, Kuhnt W, Holbourn A. 2004. Foraminiferal response to sea level change, organic flux and oxygen deficiency in the Cenomanian of the Tarfaya Basin, southern Morocco. Marine Micropaleontology, 53(1–2): 133–157, doi: 10.1016/j.marmicro.2004.05.007
Gong Zaisheng, Jin Qinghuan, Qiu Zhongjian, et al. 1989. Geology, tectonics and evolution of the Pearl River Mouth Basin. In: Zhu X, ed. Chinese Sedimentary Basins. Amsterdam: Elsevier, 181–196
Gourley T L, Gallagher S J. 2004. Foraminiferal biofacies of the Miocene warm to cool climatic transition in the Port Phillip Basin, southeastern Australia. Journal of Foraminiferal Research, 34(4): 294–307, doi: 10.2113/34.4.294
Gradstein F M, Ogg J G, Schmitz M D, et al. 2012. The Geologic Time Scale 2012. Amsterdam: Elsevier, 1083–1094
Gupta A K. 1997. Paleoceanographic and paleoclimatic history of the Somali Basin during the Pliocene-Pleistocene; Multivariate analyses of benthic foraminifera from DSDP Site 241 (Leg 25). Journal of Foraminiferal Research, 27(3): 196–208, doi: 10.2113/gsjfr.27.3.196
Gupta A K, Das M. 2007. Occurrence of the biogenic bloom in the oligotrophic southeastern Indian Ocean: evidence from the late Neogene deep-sea benthic foraminifera (ODP Hole 752A). Journal Geological Society of India, 69(2): 331–343
Gupta B K S, Platon E, Bernhard J M, et al. 1997. Foraminiferal colonization of hydrocarbon-seep bacterial mats and underlying sediment, Gulf of Mexico slope. Journal of Foraminiferal Research, 27(4): 292–300, doi: 10.2113/gsjfr.27.4.292
Gupta L P, Kawahata H. 2006. Downcore diagenetic changes in organic matter and implications for paleoproductivity estimates. Global and Planetary Change, 53(1–2): 122–136, doi: 10.1016/j.gloplacha.2006.01.008
Hall R. 2012. Late Jurassic-Cenozoic reconstructions of the Indonesian region and the Indian Ocean. Tectonophysics, 570-571: 1–41, doi: 10.1016/j.tecto.2012.04.021
Hammer Ø, Harper D A T, Ryan P D. 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4(1): 1–9
Hao Yichun, Qiu Songyu, Lin Jiaxing, et al. 1980. Foraminifera (in Chinese). Beijing: China Science Publishing and Media Ltd, 1–224
Haq B U, Hardenbol J, Vail P R. 1987. Chronology of fluctuating sea levels since the Triassic. Science, 235(4793): 1156–1167, doi: 10.1126/science.235.4793.1156
Hess S, Kuhnt W. 1996. Deep-sea benthic foraminiferal recolonization of the 1991 Mt. Pinatubo ash layer in the South China Sea. Marine Micropaleontology, 28(2): 171–197
Hohenegger J. 2005. Estimation of environmental paleogradient values based on presence/absence data: a case study using benthic foraminifera for paleodepth estimation. Palaeogeography, Palaeoclimatology, Palaeoecology, 217(1–2): 115–130, doi: 10.1016/j.palaeo.2004.11.020
Hohenegger J, Andersen N, Báldi K, et al. 2008. Paleoenvironment of the Early Badenian (Middle Miocene) in the southern Vienna Basin (Austria)—multivariate analysis of the Baden-Sooss section. Geologica Carpathica, 59: 461–487
Holbourn A, Henderson A S, Macleod N. 2013. Atlas of Benthic Foraminifera. Chichester: Wiley, 1–641
Holbourn A, Kuhnt W, Schulz M. 2004. Orbitally paced climate variability during the middle Miocene: high resolution benthic foraminiferal stable-isotope records from the tropical western Pacific. In: Clift P, Kuhnt W, Wang Pinxian, et al., eds. Continent–Ocean Interactions Within East Asian Marginal Seas. Washington: American Geophysical Union, 321–337
Holbourn A, Kuhnt W, Schulz M, et al. 2007. Orbitally-paced climate evolution during the middle Miocene “Monterey” carbon-isotope excursion. Earth and Planetary Science Letters, 261(3–4): 534–550, doi: 10.1016/j.jpgl.2007.07.026
Huang Chiyue. 1989. Implication of the Post-Lushanian faunal change for the occurrence of Kuroshio Current in the early late Miocene: foraminiferal evidence from the Chuhuangkeng section, northern Taiwan. Proceedings of the Geological Society of China, 32: 21–45
Huang Chiyue, Yen Yi, Zhao Quanhong, et al. 2012. Cenozoic stratigraphy of Taiwan: window into rifting, stratigraphy and paleoceanography of South China Sea. Chinese Science Bulletin, 57(24): 3130–3149, doi: 10.1007/s11434-012-5349-y
Hubei Institute of Geosciences. 1978. Paleontological Atlas of Southwest China (Volume of Microfossils)(in Chinese). Beijing: Geological Publishing House, 1–115
Jiang Zhongxiong, Zeng Lin, Li Mingxing, et al. 1994. The North Continental Shelf Region of South China Sea. Tertiary in Petroliferous Regions of China (in Chinese), vol. 8. Beijing: Petroleum Industry Press, 1–145
Jones R W. 1994. The Challenger Foraminifera. New York: Oxford University Press, 149
Jorissen F J. 1987. The distribution of benthic foraminifera in the Adriatic Sea. Marine Micropaleontology, 12: 21–48, doi: 10.1016/0377-8398(87)90012-0
Jorissen F J, de Stigter H C, Widmark J G V. 1995. A conceptual model explaining benthic foraminiferal microhabitats. Marine Micropaleontology, 26(1–4): 3–15, doi: 10.1016/0377-8398(95)00047-X
Jorissen F J, Fontanier C, Thomas E. 2007. Chapter seven paleoceanographical proxies based on deep-sea benthic foraminiferal assemblage characteristics. Developments in Marine Geology, 1: 263–325, doi: 10.1016/S1572-5480(07)01012-3
Kaiho K. 1994. Benthic foraminiferal dissolved-oxygen index and dissolved-oxygen levels in the modern ocean. Geology, 22(8): 719–722, doi: 10.1130/0091-7613(1994)022<0719:BFDOIA>2.3.CO;2
Kaiho K. 1999. Effect of organic carbon flux and dissolved oxygen on the benthic foraminiferal oxygen index (BFOI). Marine Micropaleontology, 37(1): 67–76, doi: 10.1016/S0377-8398(99)00008-0
Kamikuri S I, Moore T C. 2017. Reconstruction of oceanic circulation patterns in the tropical Pacific across the early/middle Miocene boundary as inferred from radiolarian assemblages. Palaeogeography, Palaeoclimatology, Palaeoecology, 487: 136–148, doi: 10.1016/j.palaeo.2017.08.028
Kamikuri S I, Motoyama I, Nishi H, et al. 2009. Evolution of eastern pacific warm pool and upwelling processes since the middle Miocene based on analysis of radiolarian assemblages: response to Indonesian and Central American seaways. Palaeogeography, Palaeoclimatology, Palaeoecology, 280(3-4): 469–479, doi: 10.1016/j.palaeo.2009.06.034
Katz M E, Miller K G, Mountain G S. 2003. Biofacies and lithofacies evidence for paleoenvironmental interpretations of upper Neogene sequences on the New Jersey continental shelf (ODP LEG 174A). In: Olson H C, Leckie R M, eds. Micropaleontologic Proxies for Sea-Level Change and Stratigraphic Discontinuities. SEPM (Society for Sedimentary Geology) Special Publication, 75: 131–146,
Kennett J P, Keller G, Srinivasan M S. 1985. Miocene planktonic foraminiferal biogeography and paleoceanographic development of the Indo-Pacific region. In: Kennett J P, ed. The Miocene Ocean: Paleoceanography and Biogeography. Boulder: Geological Society of America, 197–236
Kitazato H. 1994. Foraminiferal microhabitats in four marine environments around Japan. Marine Micropaleontology, 24(1): 29–41, doi: 10.1016/0377-8398(94)90009-4
Klovan J E, Imbrie J. 1971. An algorithm and FORTRAN-IV program for large-Scale Q-mode factor analysis and calculation of factor scores. Journal of the International Association for Mathematical Geology, 3(1): 61–77, doi: 10.1007/BF02047433
Koho K A, García R, de Stigter H C, et al. 2008. Sedimentary labile organic carbon and pore water redox control on species distribution of benthic foraminifera: a case study from Lisbon-Setúbal Canyon (southern Portugal). Progress in Oceanography, 79(1): 55–82, doi: 10.1016/j.pocean.2008.07.004
Kouwenhoven T J, van der Zwaan G J. 2006. A reconstruction of late Miocene Mediterranean circulation patterns using benthic foraminifera. Palaeogeography, Palaeoclimatology, Palaeoecology, 238(1–4): 373–385, doi: 10.1016/j.palaeo.2006.03.035
Kuhnt W, Hess S, Jian Zhimin. 1999. Quantitative composition of benthic foraminiferal assemblages as a proxy indicator for organic carbon flux rates in the South China Sea. Marine Geology, 156(1–4): 123–157, doi: 10.1016/S0025-3227(98)00176-5
Kuhnt W, Holbourn A, Hall R, et al. 2004. Neogene history of the Indonesian Throughflow. In: Clift P, Kuhnt W, Wang Pinxian, et al, eds. Continent-Ocean Interactions Within East Asian Marginal Seas. Washington: AGU, 299–320
Levin L A, Gage J D. 1998. Relationships between oxygen, organic matter and the diversity of bathyal macrofauna. Deep Sea Research Part II: Topical Studies in Oceanography, 45(1–3): 129–163, doi: 10.1016/S0967-0645(97)00085-4
Li Xuejie, Chen Fang, Chen Chaoyun, et al. 2004a. Quantitative research on relationship between planktonic foraminifera content and water depth in western South China Sea. Journal of Palaeogeography (in Chinese), 6(4): 442–447
Li Baohua, Jian Zhimin. 2001. Evolution of planktonic foraminifera and thermocline in the southern South China Sea since 12 Ma (ODP–184, Site 1143). Science in China Series D: Earth Sciences, 44(10): 889–896, doi: 10.1007/BF02907080
Li Baohua, Wang Jiliang, Huang Baoqi, et al. 2004b. South China Sea surface water evolution over the last 12 Myr: a south-north comparison from Ocean Drilling Program Sites 1143 and 1146. Paleoceanography, 19(1): PA1009
Li Tao, Xiang Rong, Li Tuanjie. 2011. Benthic foraminiferal distribution in surface sediments of Zhujiang Estuary and its environmental implications. Marine Geology & Quaternary Geology (in Chinese), 31(6): 91–98
Loeblich A R, Tappan H. 1994. Foraminifera of the Sahul shelf and Timor Sea. Cushman Foundation for Foraminiferal Research, Special Publication, 31: 661
Loubere P, Fariduddin M. 1999. Benthic Foraminifera and the flux of organic carbon to the seabed. In: Gupta B K S, ed. Modern Foraminifera. Dordrecht: Springer, 181–199
Lutze G F, Coulbourn W T. 1984. Recent benthic foraminifera from the continental margin of northwest Africa: community structure and distribution. Marine Micropaleontology, 8(5): 361–401, doi: 10.1016/0377-8398(84)90002-1
Melki T, Kallel N, Fontugne M. 2010. The nature of transitions from dry to wet condition during sapropel events in the Eastern Mediterranean Sea. Palaeogeography, Palaeoclimatology, Palaeoecology, 291(3–4): 267–285, doi: 10.1016/j.palaeo.2010.02.039
Melki T, Kallel N, Jorissen F J, et al. 2009. Abrupt climate change, sea surface salinity and paleoproductivity in the western Mediterranean Sea (Gulf of Lion) during the last 28 kyr. Palaeogeography, Palaeoclimatology, Palaeoecology, 279(1–2): 96–113, doi: 10.1016/j.palaeo.2009.05.005
Milker Y. 2010. Western Mediterranean shelf foraminifera: recent distribution, Holocene sea-level reconstructions, and paleoceanographic implications [dissertation]. Hamburg: Universität Hamburg
Miller K G, Wright J D, Fairbanks R G. 1991. Unlocking the Ice House: Oligocene-Miocene oxygen isotopes, eustasy, and margin erosion. Journal of Geophysical Research, 96(B4): 6829–6848, doi: 10.1029/90JB02015
Minhat F I, Satyanarayana B, Husain M L, et al. 2016. Modern benthic foraminifera in subtidal waters of Johor: implications for holocene sea-level change on the east coast of Peninsular Malaysia. Journal of Foraminiferal Research, 46(4): 347–357, doi: 10.2113/gsjfr.46.4.347
Mojtahid M, Griveaud C, Fontanier C, et al. 2010. Live benthic foraminiferal faunas along a bathymetrical transect (140–4800 m) in the Bay of Biscay (NE Atlantic). Revue De Micropaléontologie, 53(3): 139–162, doi: 10.1016/j.revmic.2010.01.002
Mojtahid M, Jorissen F, Lansard B, et al. 2009. Spatial distribution of live benthic foraminifera in the Rhône prodelta: faunal response to a continental-marine organic matter gradient. Marine Micropaleontology, 70(3–4): 177–200, doi: 10.1016/j.marmicro.2008.12.006
Murray J W. 1991. Ecology and Palaeoecology of Benthic Foraminifera. London: Longman Scientific and Technical, 323–326
Murray J W. 2006. Ecology and Applications of Benthic Foraminifera. Cambridge: Cambridge University Press, 327–343
Pérez-Asensio J N, Aguirre J, Schmiedl G, et al. 2012. Messinian paleoenvironmental evolution in the lower Guadalquivir Basin (SW Spain) based on benthic foraminifera. Palaeogeography, Palaeoclimatology, Palaeoecology, 326–328: 135–151, doi: 10.1016/j.palaeo.2012.02.014
Qin Guoquan. 1996. Application of micropaleontology to the sequence stratigraphic studies of Late Cenozoic in the Zhujiang River Mouth Basin. Marine Geology & Quaternary Geology (in Chinese), 16(4): 1–18
Qu Tangdong. 2000. Upper-layer circulation in the South China Sea. Journal of Physical Oceanography, 3(6): 1450–1460
Rasmussen T L, Thomsen E. 2017. Ecology of deep-sea benthic foraminifera in the North Atlantic during the last glaciation: food or temperature control. Palaeogeography, Palaeoclimatology, Palaeoecology, 472: 15–32, doi: 10.1016/j.palaeo.2017.02.012
Rathburn A E, Corliss B H. 1994. The ecology of living (stained) deep-sea benthic foraminifera from the Sulu Sea. Paleoceanography, 9(1): 87–150, doi: 10.1029/93PA02327
Rosoff D B, Corliss B H. 1992. An analysis of recent deep-sea benthic foraminiferal morphotypes from the Norwegian and Greenland seas. Palaeogeography, Palaeoclimatology, Palaeoecology, 91(1–2): 13–20, doi: 10.1016/0031-0182(92)90028-4
Sanders H L. 1969. Benthic marine diversity and the stability-time hypothesis. Brookhaven Symposia Biology, 22: 71–81
Schmiedl G, de Bovée F, Buscail R, et al. 2000. Trophic control of benthic foraminiferal abundance and microhabitat in the bathyal Gulf of Lions, western Mediterranean Sea. Marine Micropaleontology, 40(3): 167–188, doi: 10.1016/S0377-8398(00)00038-4
Schmiedl G, Kuhnt T, Ehrmann W, et al. 2010. Climatic forcing of eastern Mediterranean deep-water formation and benthic ecosystems during the past 22 000 years. Quaternary Science Reviews, 29(23–24): 3006–3020, doi: 10.1016/j.quascirev.2010.07.002
Schmiedl G, Mackensen A. 1997. Late Quaternary paleoproductivity and deep water circulation in the eastern South Atlantic Ocean: evidence from benthic foraminifera. Palaeogeography, Palaeoclimatology, Palaeoecology, 130(1–4): 43–80, doi: 10.1016/S0031-0182(96)00137-X
Schönfeld J. 1997. The impact of the Mediterranean Outflow Water (MOW) on benthic foraminiferal assemblages and surface sediments at the southern Portuguese continental margin. Marine Micropaleontology, 29(3–4): 211–236, doi: 10.1016/S0377-8398(96)00050-3
Schönfeld J. 2002. Recent benthic foraminiferal assemblages in deep high-energy environments from the Gulf of Cadiz (Spain). Marine Micropaleontology, 44(3–4): 141–162, doi: 10.1016/S0377-8398(01)00039-1
Sgarrella F, di Donato V, Sprovieri R. 2012. Benthic foraminiferal assemblage turnover during intensification of the Northern Hemisphere glaciation in the Piacenzian Punta Piccola section (Southern Italy). Palaeogeography, Palaeoclimatology, Palaeoecology, 333-334: 59–74, doi: 10.1016/j.palaeo.2012.03.009
Singh A D, Rai A K, Verma K, et al. 2015. Benthic foraminiferal diversity response to the climate induced changes in the eastern Arabian Sea oxygen minimum zone during the last 30 ka BP. Quaternary International, 374: 118–125, doi: 10.1016/j.quaint.2014.11.052
Singh R K, Gupta A K, Das M. 2012. Paleoceanographic significance of deep-sea benthic foraminiferal species diversity at southeastern Indian Ocean Hole 752A during the Neogene. Palaeogeography, Palaeoclimatology, Palaeoecology, 361–362: 94–103, doi: 10.1016/j.palaeo.2012.08.008
Smart C W, Thomas E, Ramsay A T S. 2007. Middle-late Miocene benthic foraminifera in a western equatorial Indian Ocean depth transect: paleoceanographic implications. Palaeogeography, Palaeoclimatology, Palaeoecology, 247(3–4): 402–420, doi: 10.1016/j.palaeo.2006.11.003
Speijer R P, Schmitz B. 1998. A benthic foraminiferal record of Paleocene sea level and trophic/redox conditions at Gebel Aweina, Egypt. Palaeogeography, Palaeoclimatology, Palaeoecology, 137(1–2): 79–101, doi: 10.1016/S0031-0182(97)00107-7
Szarek R, Nomaki H, Kitazato H. 2007. Living deep-sea benthic foraminifera from the warm and oxygen-depleted environment of the Sulu Sea. Deep Sea Research Part II: Topical Studies in Oceanography, 54(1–2): 145–176, doi: 10.1016/j.dsr2.2006.02.017
Székely S F, Filipescu S. 2016. Biostratigraphy and paleoenvironments of the Late Oligocene in the north-western Transylvanian Basin revealed by the foraminifera assemblages. Palaeogeography, Palaeoclimatology, Palaeoecology, 449: 484–509, doi: 10.1016/j.palaeo.2016.02.043
Takata H, Nomura R, Khim B K. 2010. Response of abyssal benthic foraminifera to mid-Oligocene glacial events in the eastern Equatorial Pacific Ocean (ODP Leg 199). Palaeogeography, Palaeoclimatology, Palaeoecology, 292(1–2): 1–11, doi: 10.1016/j.palaeo.2010.03.021
Thunell R, Belyea P. 1982. Neogene planktonic foraminiferal biogeography of the Atlantic ocean. Micropaleontology, 28(4): 381–398, doi: 10.2307/1485451
Tripati A K, Roberts C D, Eagle R A. 2009. Coupling of CO2 and ice sheet stability over major climate transitions of the last 20 million years. Science, 326(5958): 1394–1397, doi: 10.1126/science.1178296
van Hinsbergen D J J, Kouwenhoven T J, van der Zwaan G J. 2005. Paleobathymetry in the backstripping procedure: correction for oxygenation effects on depth estimates. Palaeogeography, Palaeoclimatology, Palaeoecology, 221(–-4): 245–265, doi: 10.1016/j.palaeo.2005.02.013
Vieira F S, Machado Koutsoukos E A, Machado A J, et al. 2015. Biofaciological zonation of benthic foraminifera of the continental shelf of Campos Basin, SE Brazil. Quaternary International, 377: 18–27, doi: 10.1016/j.quaint.2014.12.020
Vincent E, Berger W H. 1985. Carbon dioxide and polar cooling in the Miocene: the Monterey hypothesis. In: Sundquist E T, Broecker W S, eds. The Carbon Cycle and Atmospheric CO2: Natural Variations Archean to Present. Washington: American Geophysical Union, 455–468
Vincent E, Killingley J, Berger W H. 1985. Miocene oxygen and carbon isotope stratigraphy of the tropical Indian Ocean. In: Kennett J P, ed. The Miocene Ocean: Paleoceanography and Biogeography. Boulder: Geological Society of America, 103–130
Wade B S, Bown P R. 2006. Calcareous nannofossils in extreme environments: the Messinian Salinity Crisis, Polemi Basin, Cyprus. Palaeogeography, Palaeoclimatology, Palaeoecology, 233(3–4): 271–286, doi: 10.1016/j.palaeo.2005.10.007
Wan Xiaoqiao, Pan Zuyin, Sun Yuxiao. 1996. Neogene foraminiferal assemblages and paleoproductivity from Well PY33–1–1. In: Research on Micropalaeontology and Paleoceanography in the Pearl River Mouth Basin, South China Sea (in Chinese). Wuhan: China University of Geology Press, 88–98
Wang Pinxian. 1985. Marine Micropaleontology of China. Berlin: Spinger, 370
Wang Pinxian, He Yan, Hu Lanying, et al. 1981. Foraminifera. Petroleum Exploration Company of Chinese (South China Sea Branch)(in Chinese). Guangzhou: Guangdong Science and Technology Press, 83–137
Wang Pinxian, Li Qianyu. 2009. The South China Sea. Dordrecht: Springer, 32–34, 116, 408
Wang Pinxian, Min Qiubao, Bian Yunhua, et al. 1986. Planktonic foraminifera in the continental slope of the northern South China Sea during the last 130,000 years and their paleo-ceanographic implications. Acta Geologica Sinica (English Edition), 60(3): 1–11
Wang Pinxian, Zhang Jijun, Zhao Quanhong, et al. 1988. Distribution of Foraminifera and Ostracoda in sediment cores and paleogeography of the East China Sea (in Chinese). Beijing: China Ocean Press, 105–114
Wang Pinxian, Zhao Quanhong, Jian Zhimin, et al. 2003. Thirty million year deep sea records in the South China Sea. Chinese Science Bulletin, 48(23): 2524–2535, doi: 10.1007/BF03037016
Woodruff F, Savin S. 1991. Mid-Miocene isotope stratigraphy in the deep sea: High-resolution correlations, paleoclimatic cycles, and sediment preservation. Paleoceanography, 6(6): 755–806, doi: 10.1029/91PA02561
Wright J D, Miller K G, Fairbanks R G. 1992. Early and middle Miocene stable isotopes: implications for deepwater circulation and climate. Paleoceanography, 7(3): 357–389, doi: 10.1029/92PA00760
Wyrtki K. 1961. Physical oceanography of the Southeast Asian waters. La Jolla, CA: NAGA, 1–195
Xie Hui, Zhou Di, Li Yuanping, et al. 2014. Cenozoic tectonic subsidence in deepwater sags in the Pearl River Mouth Basin, northern South China Sea. Tectonophysics, 615–616: 182–198, doi: 10.1016/j.tecto.2014.01.010
Xu Yulin. 1996. Tertiary calcareous nannofossil zones and paleoceanographic environments of Pearl River Mouth Basin. In: Research on Micropalaeontology and Paleoceanography in the Pearl River Mouth Basin, South China Sea (in Chinese). Wuhan: China University of Geology Press, 74–87
Xue Liyuan, Ding Xuan, Pei Renjie, et al. 2018. Miocene evolution of paleo-water depth and subsidence revealed in Well LF14 from Lufeng Sag, northern South China Sea (in Chinese). Journal of Tropical Oceanography , 37(2): 72–83
Xue Liyuan, Ding Xuan, Wan Xiaoqiao. 2017. Research on the Miocene planktonic foraminferal biochrono- straitigraphy at well LF14 in the Lufeng Sag, northern South China Sea (in Chinese). Acta Micropalaeontologica Sinica, 34(3): 320–331
Yao Bochu, Zeng Weijun, Hayes D E. 1994. The Geological Memoir of South China Sea Jointly by China and USA (in Chinese). Wuhan: China University of Geosciences Press, 204
Youssef M, Taha S. 2013. Biostratigraphy and Paleoecology of Paleocene/Eocene (P/E) interval of some geological sections in Central Egypt. Arabian Journal of Geosciences, 6(11): 4279–4298, doi: 10.1007/s12517-012-0692-5
Zachos J, Pagani M, Sloan L, et al. 2001. Trends, rhythms, and aberrations in global climate 65 Ma to present. Science, 292(5517): 686–693, doi: 10.1126/science.1059412
Zeng Qingbo, Zhang Gongchen, Liao Zongbao, et al. 2015. Geological feature and prospecting potential of early Miocene platform margin belt in Dongsha Uplift, Zhujiangkou Basin. Marine Origin Petroleum Geology (in Chinese), 20(1): 17–24
Zhao Quanhong, Jian Zhimin, Wang Jiliang, et al. 2001a. Neogene oxygen isotopic stratigraphy, ODP Site 1148, northern South China Sea. Science in China Series D: Earth Sciences, 44(10): 934–942, doi: 10.1007/BF02907086
Zhao Quanhong, Wang Pinxian, Cheng Xinrong, et al. 2001b. Records of the “carbon shift” event in the South China Sea. Science in China Series D: Earth Sciences, 31(10): 808–815
Zheng Shouyi. 1988. The agglutinated and porcelanecus foraminifera of the East China Sea (in Chinese). Beijing: Science Press, 1–337
Appendix
Less
Year 2019 volume 38 Issue 3
PDF
41
23
Cite this Article
BibTeX
Article Info
doi: 10.1007/s13131-019-1405-7
  • Receive Date：2018-09-07
  • Online Date：2026-03-31
  • Published：2019-03-25
Article Data
Affiliations
History
  • Received：2018-09-07
  • Accepted：2018-12-24
Funding
The National Natural Science Foundation of China under contract No. 91328201.
Affiliations
    1 School of Ocean Sciences, China University of Geosciences, Beijing 100083, China
    2 School of Earth Sciences and Resources, China University of Geosciences, Beijing 100083, China

Corresponding:

References
Share
https://castjournals.cast.org.cn/joweb/aos/EN/10.1007/s13131-019-1405-7
Share to
QR

Scan QR to access full text

Cite this article
BibTeX
Citations
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
关闭全屏
  • BibTeX
  • EndNote
  • RefWorks
  • TxT
Links
Articles
Latest Articles
Most Read
Collections
Updates
Events
News
Multimedia
About
About Us
Contact
No. 86 Xueyuan South Road, Haidian District, Beijing
100081
010-62199257
qkjq@cast.org.cn

Copyright © 2025 China Association for Science and Technology. All rights reserved. For all open access content, the relevant licensing terms apply.
Sponsored by the Office of the Leading Group for Cybersecurity and Informatization of CAST, and supported by Science and Technology Review Publishing House