Fluxes and isotopic composition of planktonic foraminifera off Hainan Island, northern South China Sea: Implications for paleoceanographic studies

Fluxes and isotopic composition of planktonic foraminifera off Hainan Island, northern South China Sea: Implications for paleoceanographic studies

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Fluxes and isotopic composition of planktonic foraminifera off Hainan Island, northern South China Sea: Implications for paleoceanographic studies Ismail Adejare Ladigbolu a,b,c , Bao-Hua Li d , Hong-Liang Li b , Martin G. Wiesner b , Zhou-Fei Yu d , Jing-Jing Zhang b , Lin Sun a,b , Li-Hua Ran b , Ying Ye a , Jian-Fang Chen b,∗ b

a Department of Marine Science, Ocean College, Zhejiang University, Hangzhou 316021, China Key Laboratory of Marine Ecosystem and Biogeochemistry, State Oceanic Administration and Second Institute of Oceanography, Ministry of Natural Resources, Hangzhou 310012, China c Nigerian Institute for Oceanography and Marine Research, Lagos, P.M.B 12729, Nigeria d CAS Key Laboratory of Economic Stratigraphy and Palaeogeography, Nanjing Institute of Geology and Palaeontology and Center for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Nanjing 210008, China

Received 25 December 2018; received in revised form 23 April 2019; accepted 12 July 2019

Abstract Planktonic foraminifera collected from a sediment trap deployed off Hainan in the northwestern South China Sea (SCS-NW) between July 2012 and April 2013 were studied to evaluate their seasonal variability and ecology as well as to infer the factors controlling their shell fluxes. The total planktonic foraminifera flux, as well as the fluxes of the dominant species (Globigerinoides ruber, Globigerinoides sacculifer and Neogloboquadrina dutertrei), showed three distinct maxima during SW-monsoon in August 2012, the SW-NE intermonsoon in October 2012 and the NE-monsoon in December 2012–February 2013. These periods were characterized by upwelling, aerosol fallout, and intense wind mixing, respectively, from which the foraminiferal assemblages benefitted, as indicated by the close correlation between wind speed, sea surface temperature (SST), chlorophyll a concentration (Chl-a), δ18 O of G. ruber and the shell fluxes. The correlation also suggests that temperature and food availability might have been the primary drivers of the observed changes in foraminiferal abundance. The offset between the SST deduced from flux-weighted of G. ruber δ18 O and annual mean SST is only ∼0.3 ◦ C, much lower than ∼5.2 ◦ C between the summer and winter temperature, indicating a balanced seasonality bias in the shell flux. The linear regression between the satellite-derived sea surface temperature and G. ruber δ18 O reveals the strong potential of this species, at least in the studied region, as an ecological indicator for past oceanic environments. © 2019 Published by Elsevier B.V. on behalf of Nanjing Institute of Geology and Palaeontology, CAS. Keywords: Planktonic foraminifera; Sediment trap flux; Stable isotope; Seasonality; Northwestern South China Sea

1. Introduction The most commonly used proxies in the study of paleoceanography include the planktonic foraminiferal assemblages, the stable oxygen and carbon isotopes as well as trace-element composition of their shells (Lea, 1999; Rohling and Cooke, 1999), and the composition of their shell-bound organic matter (King and Hare, 1972a, 1972b; Langer et al., 1993; Stathoplos and Tuross, 1994; Uhle et al., 1997). These are applied to generate quantitative estimates of ocean boundary conditions, such as the sea surface temperature (SST), salinity (SSS), and those ∗

of biotic response, including primary production and carbon flux. These proxies from planktonic foraminifera are widely used in paleoceanographic studies, not only because of their assemblages that vary with marine environmental changes but also because of the ability of their shells to preserve useful information about the upper oceans in which they once lived. In the past decades, oceanic parameters have been established by the abundance of planktonic foraminifera, the stable oxygen and carbon isotope compositions of their shells for temperature, upwelling, nutrient enrichment, and productivity. However, these paleoceanographic signals present in the foraminiferal shell could be affected by physiological effects and create both “oxygen” and

Corresponding author. E-mail address: [email protected] (J.F. Chen).

https://doi.org/10.1016/j.palwor.2019.07.006 1871-174X/© 2019 Published by Elsevier B.V. on behalf of Nanjing Institute of Geology and Palaeontology, CAS.

Please cite this article in press as: Ladigbolu, I.A., et al., Fluxes and isotopic composition of planktonic foraminifera off Hainan Island, northern South China Sea: Implications for paleoceanographic studies. Palaeoworld (2019), https://doi.org/10.1016/j.palwor.2019.07.006

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“carbon” isotope disequilibrium relative to the ambient seawater (Niebler et al., 1999). Therefore, a good knowledge of ecology, life cycle, and shell calcification processes of the individual foraminiferal species is required for better interpretation of the fossil record (Niebler et al., 1999). For instance, Globigerinoides ruber is a mixed layer subtropical and tropical species, and a good recorder of near-surface temperature because of its low-slope response to a deepening isotherm (high insulation for the low temperature at depth compared to other species). This makes it a good species for surface water temperature reconstruction (Field, 2004; Tedesco et al., 2007; Wejnert et al., 2010). Seasonal variation in the shell flux in the three seasonality modes described by Jonkers and Kuˇcera (2015) could also serve as useful tools in the understanding and interpretation of shell-flux variability pattern, and their applicability in paleoceanographic reconstruction. For example, seasonal variation in shell flux in the warm water planktonic foraminiferal species (group A) was reported to be low within the optimal temperature range. In that case, species record average annual condition with only little offset, but outside their optimal temperature range, species concentrate a progressively large portion of their annual flux into a single peak in autumn. This often results in an increase in positive bias from mean annual conditions. Under both the cooling and warming trends, the species seasonality shifts toward an odd flux throughout the year, which will lead to underestimation of the actual changes in mean temperature (Jonkers and Kuˇcera, 2015). Recent publications on environmental investigations of the South China Sea (SCS) on the basis of planktonic foraminifera were largely focused on their seasonal and interannual variations in the central SCS (Chen et al., 2000, 2007), seasonal variability off Xisha Island (Liu et al., 2014; Xiang et al., 2015), variation in their flux and chemical properties in the southern basin (Wan et al., 2010), assemblage composition in plankton tows from the northern SCS (Lin and Hsieh, 2007), circulation and oxygenation of the glacial SCS (Li et al., 2017), in situ calibration of the Mg/Ca ratio in their shells (Huang et al., 2008), upper watercolumn structure and non-analog planktonic foraminiferal fauna in the glacial southern SCS (Steinke et al., 2008, 2010). The SCS is a highly dynamic monsoonal subregion characterized by a variety of processes that govern the fluxes of particulate matter to the deep sea. This includes massive riverine discharges of sediments and nutrients, upwelling, mesoscale eddies, dust fallout, and El Nino˜¨ -southern oscillation (ENSO) events (see Section 1.1). Therefore, because of this multiplicity, a quantitative understanding of the individual forcings controlling the distribution of planktonic foraminifera is required. The objective of this study is to improve our understanding of the ecology, seasonal variability, and possible factors mediating the shell fluxes of some observed planktonic foraminifera in the northern SCS. 1.1. Study area The South China Sea (SCS), which is the largest marginal sea in the western tropical Pacific Ocean, has an area of about

3.5 million km2 and depths ranging from the shallowest coastal region to 5567 m, with an average depth of 1212 m (Morton and Blackmore, 2001). It is located within the East Asian Monsoon system with sea surface temperature (SST) and sea surface salinity (SSS) varying between <24 ◦ C and >29 ◦ C, and 34.2 psu and 33.6 psu, during winter and summer seasons respectively in the north (Fig. 1, Locarnini et al., 2013), except for its coastal areas. It is a typical well-stratified oligotrophic sea with depleted surface nutrients, thereby manifesting low primary production in the surface layer (Wong et al., 2007; Du et al., 2017). The biogeochemistry of the SCS is responsive to multiscale physical forcings, such as intraseasonal upwelling and mesoscale eddies (Liu et al., 2002; Ning et al., 2004), the seasonally reversing monsoon, and the interannual ENSO events (Liu, H. et al., 2013). The effects may be recorded in changes in nutrient concentrations, Chl-a, primary production, and POC export. The seasonally varying hydrological characteristics of the SCS are complex (Fig. 1a). The East Asian monsoon (northeast monsoon in winter and southwest monsoon in summer) is the primary driver, resulting in a large basin-scale cyclonic upper layer circulation during winter and sub-basin-scale cyclonic and anticyclonic gyres during summer (Fig. 1a; Wyrtki, 1961). Mixed layer depth (MLD), which is modulated by wind stress and solar radiation, exhibits pronounced seasonal variability in the northern SCS (Tseng et al., 2005). Because MLD in large part determines the nutrient supply to the upper waters, primary production in this region also exhibits strong seasonal variability. In summer, strong solar radiation stratifies upper ocean layers, resulting in a shallow MLD, nutrient limitation, and reduced primary production in most of the basin. Off Hainan and along the coast southeastern Vietnam, however, the strong southwesterly winds generate upwelling during summer, thus enhancing primary production (Ning et al., 2004; Su and Pohlmann, 2009; Cai et al., 2015). In winter, in addition to the strengthened surface cooling, the monsoon enhanced wind mixing deepens the mixed layer, thus entraining nutrientladen subsurface water to the surface (Zhang et al., 2019). This results in the enhanced surface water photosynthesis and higher concentrations of Chl-a (Tseng et al., 2005). Therefore, new primary production (NPP) in the SCS basin is typically uppermost in winter, when the greatest amount of nitrate is injected into the euphotic zone (Chen, 2005). Intraseasonal events are also important. Cyclonic eddies (Tang et al., 1999; Wang et al., 2016; Zhang et al., 2019), typhoons (Liu, H. et al., 2013; Liu, K.K. et al., 2013) and internal waves (Pan et al., 2012) may all serve to upwell nutrientrich deep water to the upper ocean, thereby stimulating the phytoplankton growth and increasing the primary production. Elevated primary production has also been observed in the northern SCS during aerosol (e.g., dust) deposition events (Wong et al., 2002; Zhang et al., 2019). These events directly load bionitrogen (N) from external sources into the SCS (Krishnamurthy et al., 2007; Kim et al., 2014; Zhang et al., 2019) while also supplying iron (Fe) to stimulate nitrogen fixation (Wong et al., 2002, 2007). The extent to which these processes and their seasonal, intraseasonal, and interannual variability impact the

Please cite this article in press as: Ladigbolu, I.A., et al., Fluxes and isotopic composition of planktonic foraminifera off Hainan Island, northern South China Sea: Implications for paleoceanographic studies. Palaeoworld (2019), https://doi.org/10.1016/j.palwor.2019.07.006

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Fig. 1. Map of the South China Sea showing the location of the sediment trap SCS-NW (blue star) in this study with the distribution of the annual mean sea surface temperature (SST) during 1955–2012 (a), and corresponding monthly sea surface temperature (b), and salinity (c) at the location of the sediment trap. Red (blue) arrows indicate surface water circulation during summer (winter) season (Zhang et al., 2019); sea surface temperature and salinity are from the World Ocean Atlas database (https://data.nodc.noaa.gov/las/getUI.do; Locarnini et al., 2013).

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planktonic foraminifera shell fluxes and geochemistry is yet not fully understood.

fluxes pattern based on previous works (Chen et al., 2000; Wan et al., 2010; Xiang et al., 2015).

2. Materials and methods

2.2. Stable isotope analysis

2.1. Sampling and planktonic foraminiferal analysis

Planktonic foraminiferal δ18 Ocalcite and δ13 Ccalcite were measured from the clean shells of G. ruber (white, 200–600 ␮m). The specimens were picked and further cleaned with a fine wet brush under the binocular microscope to ensure that they were not contaminated or damaged in any form. The selected foraminiferal specimens were cleaned in methanol in an ultrasonic bath to remove adhering fine particles. The clean shells were then transferred to the measuring bottle, crushed and cleaned in methanol in an ultrasonic bath, after which they were oven dried at 50 ◦ C overnight. In general, 2–7 specimens of G. ruber were analyzed using a Finnigan MAT 253 stable isotope mass spectrometer equipped with a Kiel III carbonate device at the Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences. The standard deviation of the external reproducibility was ±0.07‰ for δ18 O and ±0.05‰ for δ13 C. The results are reported relative to Vienna Pee Dee Belemnite (PDB).

A time-series sediment trap (Mark VI) with a collection aperture area of 0.5 m2 and 21 collection cups were deployed at the water depth of 1000 m at 17.43 ◦ N, 110.47 ◦ E, off southwest Hainan in the northern South China Sea (Fig. 1a) from July 2012 to April 2013. The sediment trap is about 500 m above the seafloor; therefore, potential effects of reworked/re-suspension in our sediment sample is expected to be absent or very low. The trap was programmed to collect particulate matter at intervals of 15 days, except during December through February when samples were collected at intervals of 30 days. Before deployment, 250 ml polyethylene pre-cleaned collection cups were filled with seawater from the depth at which the trap was deployed. The seawater was filtered on a pre-combusted filter, and 35 g/l of sodium chloride (NaCl) and 3.3 g/l mercury chloride (HgCl2 ) were added to prevent water exchange between the cups and surrounding seawater (diffusion), as well as to retard microbial degradation of the trapped material. The retrieved samples were wet-sieved through a 1 mm mesh screen or nylon sieve to remove zooplankton that might have made their way into the sample bottles through the trap entrance. The >1 mm materials on the sieve screen were gently washed with a small volume of filtered seawater to separate and allow any <1 mm particles that may have adhered to the material to pass through the sieve into the <1 mm fraction. These <1 mm fractions were split into four aliquots using a high-precision rotary splitter (McLane WSD-10). One-quarter of aliquots used for planktonic foraminiferal analysis was washed through a 63 ␮m sieve, and then oven dried at 60 ◦ C. Next, 50–100 mg of the cleaned, dried samples >63 ␮m were passed through a 154 ␮m sieve. Pick-up, identification, and counting analysis of all planktonic foraminiferal species was conducted on the >154 ␮m size under the stereo-microscope following the taxonomy proposed by Bé (1977) and Hemleben et al. (1989), but only species of interest were presently reported. Fluxes (tests/m2 /day) were calculated based on the sample aliquot, the duration of each collecting period, and the size of the collecting aperture of the sediment trap (0.5 m2 ) and multiplied by the number of foraminifers counted. The daily wind speed data was derived from the Advanced SCATterometer (http://apdrc.soest.hawaii.edu). Daily surface total Chl-a were derived from the NASA Ocean Biogeochemical Model assimilated daily global satellite Chl-a product, with a horizontal resolution of 0.67◦ × 1.25◦ (https://giovanni.gsfc.nasa.gov/giovanni), The Chl-a was used as an indicator of ocean primary productivity. The percentage abundance (%) of summer flux and winter flux were estimated based on the assumption that winter was from November to March while summer was from June to September. However, we assumed that the missing one or two months in summer period might not change the observed summer and winter shell

2.3. Estimation of the seawater δ18 Ow from salinity Since no conductivity, temperature and depth (CTD) device was cast during our investigation, we made use of the sea temperature, salinity, and depth profile data for the area around the study site (17.612 ◦ N–20.028 ◦ N, 111.173 ◦ E–117.989 ◦ E). That was made available by the ARGO biological and hydrological projects data unit of the Second Institute of Oceanography, Hangzhou, China, except July and August 2012, when no data were available for our study area. The SCS modern salinity-δ18 Ow relationship (Su, 2000; Lin, 2000; Lin et al., 2003) established for coastal seawater was adopted for calculating the seawater δ18 Ow as follow: δ18 Ow = −11.6 + 0.33 × S where S is the measured salinity (psu), and δ18 Ow is the seawater oxygen isotope (‰, SMOW). 3. Results 3.1. Planktonic foraminiferal flux The total planktonic foraminifera flux (TPFF) shows three distinct maxima during SW-monsoon in August 2012 (850 tests/m2 /day), the SW-NE intermonsoon in October 2012 (1150 tests/m2 /day) and the NE-monsoon in December 2012–February 2013 (545 tests/m2 /day) (Fig. 2). The average flux for the sampling period is about 328 tests/m2 /day. Among the six key species analyzed, G. ruber accounts for 29%, Globigerinoides sacculifer for 51%, and Neogloboquadrina dutertrei for 14% of the TPFF. About 50–60% of the annual average flux of G. ruber, G. sacculifer and N. dutertrei occurred in the winter season while this percentage was only around 15% for the summer (Fig. 7).

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Fig. 2. The total planktonic foraminifera flux histogram at different collection periods (tests/m2 /day) in the study site. Red, summer; black, winter; gray, autumn and spring.

Fig. 3. Comparison of six planktonic foraminifera shell fluxes (tests/m2 /day), sea surface temperature (SST, ◦ C), chlorophyll a concentration (Chl-a, ␮g/m3 ) and G. ruber δ18 O (‰, PDB) at different collection periods.

The abundance of Globigerinella siphonifera was about 6.2% of the TPFF, and its highest flux rate was attained during the aerosol deposition event in October 2012 (110 tests/m2 /day)

(Figs. 2, 3). Orbulina universa and Globorotalia menardii made up about 0.4% and 0.8% of the TPFF, respectively, and displayed similar flux patterns with flux maxima in November

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Fig. 4. Salinity (a) and temperature (b) profile from Argo float in the uppermost 250 m water column near the trap site from September 2012 to April 2013, seawater δ18 Osw (c) calculated from salinity using Lin et al. (2003)’s equation (gray dash line represents the average calculated seawater δ18 Osw ), and comparison of the satellite SST with G. ruber δ18 O (‰, PDB) at the trap site (d).

2012 (9 and 20 tests/m2 /day, respectively) and March 2013 (5 and 10 tests/m2 /day, respectively) (Fig. 3). 85–95% of the average annual flux of the three species fall upon the winter season, whereas none of these species was observed in the summer (Fig. 7).

3.2. Seasonality of planktonic foraminiferal species The seasonal flux variation of the surface-dwelling species G. ruber and G. sacculifer followed the pattern of total planktonic foraminifera flux (TPFFs) (Figs. 2, 3). The only slight difference was that the highest flux for G. ruber was observed in late October, while that of G. sacculifer was in mid-late August. N. dutertrei, a common thermocline dwelling species, showed a similar seasonal flux distribution as G. ruber, with prominent peaks occurring at almost the same period. O. universa was only observed in mid-November, early December, and early to mid-April, with the highest flux in mid-November (Fig. 3). G. siphonifera shell flux was observed during six sampling periods, with the highest amount observed in mid-late October of 2012. G. menardii exhibited similar patterns with O. universa in shell flux, and their peak fluxes were observed in the same period except for a one-month delay of G. menardii during January compared to O. universa (Fig. 3).

Table 1 δ18 O and δ13 C in planktonic foraminiferal species G. ruber. Start of collection

End of collection

7/22/2012 8/6/2012 8/6/2012 8/21/2012 8/21/2012 9/5/2012 9/20/2012 9/5/2012 10/5/2012 9/20/2012 10/5/2012 10/20/2012 11/4/2012 10/20/2012 11/19/2012 11/4/2012 11/19/2012 12/4/2012 1/3/2013 12/4/2012 2/2/2013 1/3/2013 2/2/2013 3/4/2013 4/3/2013 3/19/2013 4/18/2013 4/3/2013 4/18/2013 4/26/2013 Average (standard deviation) Flux weighted (standard deviation)

δ18 O (‰ VPDB)

δ13 C (‰ VPDB)

−3.316 −2.549 −2.594 −3.115 −2.894 −3.019 −2.892 −2.888 −2.543 −2.858 −2.29 −2.096 −2.11 −2.459 −2.309 −2.66 (±0.37) −2.76 (±0.15)

0.593 −0.198 −0.528 0.426 0.023 0.467 0.472 0.493 −0.033 0.409 0.074 −0.182 −0.977 −0.625 −0.307 0.01 (±0.46) 0.15 (±0.04)

3.3. G. ruber δ18 O and δ13 C, and seawater δ18 Ow The δ18 O of G. ruber ranged from −2.10‰ to −3.32‰ with an average value of −2.66‰, while its δ13 C values ranged from −0.98‰ to 0.59‰ (mean value of 0.01‰) (Table 1). The fluxweighted δ18 O is −2.76‰ in G. ruber with a standard deviation of less than 0.15‰. The δ18 O of G. ruber closely follows the

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Fig. 5. Plot of the satellite SST (◦ C) against the δ18 O difference (δ18 Oc –δ18 Ow ) between G. ruber test and seawater. The arrow indicates the width of difference between temperature deduced from the flux-weighted δ18 O of G. ruber and the annual mean SST.

Fig. 6. Comparison of the prevailing wind speed, sea surface temperature, chlorophyll a concentration (Chl-a), G. ruber δ18 O and planktonic foraminiferal shell flux during the study period. The dark gray and light gray shadow represents summer and winter, respectively.

SST seasonality (Fig. 4d). The heaviest δ13 C (0.593‰) and δ18 O (−2.096‰) occurred in July 2012 and February 2013, while the lightest values were observed in early April 2013 (−0.625‰) and July 2012 (−3.316‰), respectively (Table 1).

The δ18 Ow values calculated from the salinity range in the upper 50 m of the water column (33.2–33.8 psu, Fig. 4b) vary between −0.44‰ and −0.66‰ with an average of −0.54‰ (Fig. 4c). G. ruber δ18 Oc correlates well with the SST seasonality (Fig. 4d),

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observed in our investigation showed a little difference from that in the Xisha trough (465 tests/m2 /day; Xiang et al., 2015) and ∼415 tests/m2 /day of the central SCS (Chen et al., 2000), but was much lower than 704 tests/m2 /day of the southern SCS (Wan et al., 2010). The observed gap of the PF annual average flux between the present study and that of the Xisha trough might occur due to different years. Meanwhile, the observed TPFF peak at Site SCS-NW during the winter period is similar with those previously reported in the SCS (Chen et al., 2000; Wan et al., 2010; Xiang et al., 2015), which engendered the consideration that the three TPFF peaks in the present study were not very different from the already reported unimodal peaks in the Xisha trough, bimodal peaks of both the southern SCS and central SCS, as they were all monsoonal hydrographic setting related, with relevant temperature, light intensity and food availability (Figs. 3, 6). Fig. 7. Winter and summer shell flux percentage (%) of the observed six planktonic foraminiferal species at Site SCS-NW during 2012–2013. Red, summer; black, winter.

while the correlation between the SST and δ18 O difference (δ18 Oc –δ18 Ow ) between G. ruber test and seawater (in which, the water δ18 Ow was converted to PDB from SMOW by subtracting 0.27‰) reaches 0.64 (Fig. 5). The offset between the flux-weighted isotopic temperature (27.5 ◦ C) and annual mean temperature (27.2 ◦ C) is equivalent to 0.3 ◦ C. 4. Discussion In general, the peak foraminiferal flux periods with a time lag of about one collection interval coincide with the phases of the enhanced wind strength, low SST, and increases in Chla (Fig. 6). A recent study has reported the detailed variability of the major particle components (organic matter, biogenic opal, carbonate and lithogenic particles) of the same 2012–2013 timeseries trap at SCS-NW and compared with remote sensing data (Zhang et al., 2019). The August high peak in the particle flux is considered to be related to an upwelling phase off Hainan, while the October increase in bulk settling particles is due to an enhanced primary productivity in response to nutrients injection by aerosol deposition at the trap site; the winter maximum is induced by intense wind mixing and surface ocean cooling. This reveals the importance of food availability and temperature to the relatively enhanced shell flux of G. ruber, G. sacculifer, and N. dutertrei during summer, autumn, and winter. Though the sediment trap in the Xisha trough (Xiang et al., 2015) is close to present site, its uni-modal total planktonic foraminiferal shell flux is quite different from present three peaks at Site SCS-NW. Nevertheless, the higher TPFF in the Xisha trough was also reported to occur when the SST is decreasing, and Chl-a is gradually increasing just as it was observed in our study site (Fig. 6). This further alludes to the importance of temperature and food availability to the high TPFF observed in the northern SCS. The annual average flux (328 tests/m2 /day)

4.1. Summer shell flux forcing factors The high shell fluxes of G. ruber, G. sacculifer and N. dutertrei in late August 2012, the warm summer period, when sea surface temperature is 28.64 ◦ C and Chl-a 0.167 ␮g/m3 (Fig. 3) coincide with summer upwelling documented by Zhang et al. (2019) in the same site in 2012–2013. This implies the observed summer (late August 2012) high PF shell fluxes being temperature and food availability mediated. In a sensitivity study, it was reported that when the temperature and light are suitable, food availability might be the next controlling factor on planktonic foraminiferal abundance (Fraile et al., 2008). However, most of our studied species are tropical and subtropical algal symbiont-bearing species with narrow temperature tolerance, which have been considered to have little or no reliance on primary production (Caron et al., 1982; Hemleben et al., 1989; Jonkers and Kuˇcera, 2015; Schiebel and Hemleben, 2017). Though the cooling summer temperature due to the upwelling may lead cold nutrient enriched deep water to the surface ocean, and be responsible or mediate increasing shell flux of these species, temperature appears to exert the main controls on the studied planktonic foraminiferal species at Site SCS-NW (Fig. 3). The optimal temperature (thermal niches) difference of G. sacculifer (28 ◦ C) and G. ruber (>25 ◦ C, Fraile et al., 2008) may be responsible for the occurrence of the highest shell flux prominent peak of G. sacculifer during summer upwelling when the temperature was ∼28.6 ◦ C and that of G. ruber and N. dutertrei in autumn when the temperature is about 27.5 ◦ C (Fig. 3). Although the mechanism through which temperature controls phenology is still not completely understood, the most possible explanation is that every individual species have a thermal niche; a preferred temperature range that optimally balances the growth and respiration, and triggers the reproduction, which leads to ˇ c et al., 2005; the observed seasonality in the shell fluxes (Zari´ Lombard et al., 2011; Mackas et al., 2012; Jonkers et al., 2013; Jonkers and Kuˇcera, 2015).

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4.2. Seasonality of planktonic foraminiferal species During the investigation period (July 2012 to April 2013) the randomness in the flux seasonality of planktonic foraminiferal species observed in our sites in the northern SCS appears to agree well with the general pattern of seasonality in the flux of extant planktonic foraminiferal warm waters species at low latitude (Jonkers and Kuˇcera, 2015). Both G. ruber and G. sacculifer species exhibited a higher percentage (%) of the shell flux in winter- and summer- monsoon seasons compared to the intermonsoon periods. The highest fluxes in all studied species were observed during the winter (Figs. 3, 7). These observations are similar to those of Xiang et al. (2015) from the Xisha trough in the SCS, with the highest shell fluxes of both G. ruber and G. sacculifer observed during winter, which reflects the common regional hydrographic control of the planktonic foraminiferal seasonal flux. However, there is still a slight difference between the seasonal variability of shell fluxes of G. ruber and G. sacculifer, especially during the winter and late spring at Site SCS-NW (Fig. 3e, f). It is speculated that the differences in the species thermal niches (optimum temperature ranges), Chl-a, ontogenetic or synodic lunar cycle even the relationship with MLD may control the planktonic foraminiferal species abundance as suggested by Rebotim et al. (2017). N. dutertrei has higher fluxes in August, October and January at Site SCS-NW (Fig. 3d). This result is similar with the high shell flux of N. dutertrei in the central SCS, southern SCS and Xisha trough during both winter and summer monsoon periods (Chen et al., 2000; Wan et al., 2010; Xiang et al., 2015), as well as in the surface sediment of the modern Kuroshio branch (Liu et al., 2011). Investigation has shown that N. dutertrei is exclusively living on phytoplankton blooms or high primary production (Hemleben et al., 1989). Thus, the temperature may not be the most important factor, while the food availability induced by the monsoon upwelling, stronger surface water mixing and even the oceanic lateral advection (Liu et al., 2011) plays a key role on the high fluxes of N. dutertrei in the study region. The seasonal peak abundance of G. siphonifera was found to be tightly in phase or correlated with the decreasing in summer maxima temperature, but with a generally higher Chl-a and wind speed from October 2012 to January 2013 in the study region off Hainan (Figs. 3c, g, 6 b, d). This is different from the unclear seasonality of this species previously reported in Xisha trough (Xiang et al., 2015), western equatorial Pacific warm pool (Kawahata et al., 2002) and the Indian Ocean off southern Java (Mohtadi et al., 2009). G. siphonifera is commonly found in tropical and subtropical regions, usually exhibits high abundance in areas of strong currents and upwelling (Bé, 1977; Bé and Hutson, 1977; Xiang et al., 2010). This observation in the northern SCS suggests that the primary production, instead of the temperature, may be a mediating factor for the shell flux of G. siphonifera in the study region. O. universa shows a strong similarity in its shell flux abundance with G. menardii in this study (Fig. 3a, b). Its fluxes occurred only in the periods when the other observed planktonic foraminiferal species showed relatively low flux rates. The only

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difference was the appearance of G. menardii shell flux from December 4, 2012, to January 3, 2013, which is about 30 days delay than that of O. universa. 4.3. Shell δ18 Oc and flux seasonality effect The δ18 Oc of G. ruber follows the SST variation in the northern SCS (Fig. 4d). The cross-plot of G. ruber δ18 Oc with SST optimizes a linear regression (Fig. 5) as follow: SST = −2.8214(δ18 Oc -δ18 Ow ) + 21.956 Based on the equation, flux-weighted G. ruber δ18 O at Site SCS-NW corresponds to 27.5 ◦ C in temperature, which can be correlated to the satellite-derived annual mean SST of 27.2 ◦ C. This result reflects that seasonal shell fluxes of G. ruber are distributed in balance during the investigation periods, which implies that the SST deduced from flux-weighted δ18 O is close to the annual mean SST, with an error (offset) of 0.3 ◦ C. This result is similar to the offset reported by Jonkers and Kuˇcera (2015) in SCS and Fallet et al. (2010) in the Mozambique Channel upstream. The little temperature offset of 0.3 ◦ C observed in the northern SCS, is in agreement with the characteristics of warm species, G. ruber, within the optimal temperature range described by Jonkers and Kuˇcera (2015). Consequently, this study supports that G. ruber can be adopted as a good proxy for paleo-temperature reconstruction. 5. Paleoceanographic implications of the shell flux seasonal variability The planktonic foraminiferal fossil record is an important source of the physical and chemical information of the past oceans. Interpretation of foraminifera-based proxies for past environmental change is not a very straightforward task. It requires a proper understanding of the ecology of the species involved. The shells flux export of planktonic foraminifera vary spatially and temporally (Bé, 1960; Bé and Tolderlund, 1971; Deuser et al., 1981). This variability could range from timescales of less than one month (lunar) to seasonal, interannual scales and beyond, and even of several orders of magnitude (Bé and Tolderlund, 1971; Spindler et al., 1979; Deuser et al., 1981; Marchant et al., 2004). Thus, the changes in the relative abundance of species could cause the records to be weighted toward a period of maximum abundance and barring the reconstruction of the period of low relative abundances, which could largely skew the proxy signal recorded in the fossil assemblage. 5.1. How does flux variability affect planktonic foraminiferal δ18 O Due to the difference in growing periods of planktonic foraminiferal groups, the seasonal difference in shell flux could cause the flux-weighted δ18 O of the different species to represent temperature during different time of the year. It is reported that temperature offset may vary between +4 ◦ C and −4 ◦ C, even as high as 6 ◦ C in high latitude when some planktonic foraminifera

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has a summer preference; while, a negative offset usually exists for other species with a peak timing different in the temperate zone (Jonkers and Kuˇcera, 2015). Based on the temperature-δ18 O equation of Epstein et al. (1953), such a high temperature offset will result in 1–2‰ deviation in the planktonic foraminiferal shell δ18 O from different seasons (Anand et al., 2003). The high value of temperature offset has been adopted to explain the discrepancy between observed paleothermometers and climate models (Leduc et al., 2010; Laepple and Huybers, 2013; Lohmann et al., 2013; Jonkers and Kuˇcera, 2017). The seasonal difference in growing periods of planktonic foraminiferal groups will lead to an accumulative similar sedimentary difference in the δ18 O (δ18 O) (Deuser and Ross, 1989; Conan and Brummer, 2000; Hillaire-Marcel and de Vernal, 2008). Therefore, it is imperative to constrain both the vertical and seasonal distribution of planktonic foraminifera when adopting their oxygen isotope to infer the past ocean dynamics.

The seasonal flux variability of six common planktonic foraminiferal species observed at Site SCS-NW, G. ruber, G. sacculifer, N. dutertrei, O. universa, G. siphonifera and G. menardii, exhibits multi-modal peaks and can be correlated with regional monsoon strength, stronger surface water mixing and Chl-a. However, they have a relatively even flux distribution patterns during the year. This observation displays the character of the tropical and subtropical warm waters planktonic foraminiferal species, which implies that they are under the optimum temperature range. The low offset (0.3 ◦ C) between deduced temperature from the flux-weighted δ18 O (G. ruber) and mean annual temperature, and a well correlation between δ18 O and satellite SST (r = 0.64), reflect that the δ18 O of G. ruber may serve as useful proxy in reconstructing the paleo-sea surface temperature in the northern SCS.

Acknowledgments 5.2. SST seasonality in the paleoceanographic records The interspecies temperature offset, that is, the difference between one species flux-weighted δ18 O that reflects average temperature near minimum or maximum and that of another species that reflects average minimum temperature (δ18 O (max–min)) may also reveal seasonal SST, and the mechanism causing the unimodal and bimodal flux pattern of planktonic foraminifera seasonality could be assessed from the isotopic offset from equilibrium δ18 O. Our observed species strictly followed Jonker and Kuˇcera’s group A features of the three-seasonality modes, by the low offset of 0.3 ◦ C between the species flux-weighted δ18 O (G. ruber) temperature and the annual mean sea surface temperature. The closeness of temperature offset to zero, much lower than temperature difference of about ∼5.2 ◦ C between summers and winter periods, due to multi-modality and bias toward average conditions. This confirms the low seasonality effect reported for tropics (Fallet et al., 2010; Jonkers and Kuˇcera, 2015). However, at present, we cannot rule out the possibility of bias in calculated flux-weighted signal due to less than one-year time series data. Nevertheless, as it is now, our observation suggests that those planktonic foraminifera species, G. ruber, G. sacculifer and N. dutertrei, are within an optimal temperature range with low seasonal bias at Site SCS-NW (Figs. 4d, 5). Therefore, δ18 O of G. ruber may serve as a useful proxy for the reconstruction of paleo-sea surface temperature in the northern SCS. 6. Conclusions The peaks of total planktonic foraminifera flux in August, October, January, and February in the northern SCS off the Hainan Island mirrored the regional high levels of Chl-a, high wind speed and relatively light δ18 O observed in G. ruber tests. Conversely, total planktonic foraminifera flux was low in late November–early December 2012, when low Chl-a, low wind speed, and light δ18 O were observed.

This study was financially supported by the State Key Research and Development Project of China (2016YFA0601101), the Strategic Priority Research Program of the Chinese Academy of Science (XDB26000000), the National Program on Global Change and Air-Sea Interaction (GASI-03-01-03-03), the National Natural Science Foundation of China (91128212, 91528304, and 41776073) and the Special Fund for Basic Scientific Research of the Second Institute of Oceanography, Ministry of Natural Resources (JT1501, JG1514). We thank the crews of R/V Xiangyanghong-14 and R/V Tianying for their assistance in the deployment and recovery of the sediment trap moorings and the ARGO project unit of the Second Institute of Oceanography, Ministry of Natural Resources for providing seawater depth profiling in situ data. We are also grateful to Dr. Qi-Mei Guo from Nanjing Institute of Geology and Palaeontology, Chinese Academy of Science for her stupendous assistance in the laboratory analysis of the δ18 O and δ13 C isotopes. Finally, we thank Lukas Jonkers and one anonymous reviewer for their constructive comments and suggestions, which really improved this paper, Dr. Bassem Jalali for figure improvement and LetPub (www.letpub.com) for its linguistic assistance during the preparation of this manuscript.

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Please cite this article in press as: Ladigbolu, I.A., et al., Fluxes and isotopic composition of planktonic foraminifera off Hainan Island, northern South China Sea: Implications for paleoceanographic studies. Palaeoworld (2019), https://doi.org/10.1016/j.palwor.2019.07.006