Different Source Contributions of Bioactive Trace Metals in Sinking Particles in the Northern South China Sea

Abstract

Time-series samples intercepted via three synchronized moored sediment traps, deployed at 1000 m, 2150 m, and 3200 m in the northern South China Sea (NSCS) during June 2009–May 2010, were analyzed to quantify the bioactive trace metal fluxes in sinking particles and investigate their different source contributions. Iron (Fe) primarily originated from lithogenic sources. Manganese (Mn), cobalt (Co), nickel (Ni), copper (Cu), and zinc (Zn) exhibited various degrees of enrichment over their continental crustal ratios. Since the sources of bioactive trace metals in sinking particles can be divided into lithogenic, biogenic, and excess fractions, mass conservation calculations were used to quantify the contribution of each source. The results showed that Fe, Mn, and Co had extremely low biogenic proportions (0.1–3.3%), while Ni, Cu, and Zn had higher proportions (2.7–17.3%), with the biogenic fraction decreasing with the depth. Moreover, excess sources accounted for a significant proportion of Mn (68–75%), Co (34–54%), Ni (60–62%), Cu (59–74%), and Zn (56–65%) in sinking particles at the three sampling depths. The excess fractions of Mn, Co, and Cu in sinking particles can be affected by authigenic particles. This is supported by their similar scavenging-type behavior, as observed via the increase in their fluxes and enrichment patterns with the increasing depth. Furthermore, the excess fractions of Ni, Cu, and Zn may have significant contributions from anthropogenic sources. The variability of Fe in sinking particles was mainly controlled via lithogenic matter. Notably, organic matter and opal were found to be pivotal carriers in the export of excess bioactive trace metals (Mn, Co, Ni, and Cu) via the water column, accompanied with the elevated ballast effect of lithogenic matter with the depth. However, the transportation of excess Zn was more complicated due to the intricate processes involved in Zn dynamics. These findings contribute to our understanding of the sources and transport mechanisms of bioactive trace metals in the marine environment.

1. Introduction

Bioactive trace metals (such as Fe, Zn, and Cu) as life-sustaining nutrients are important in regulating biogeochemical cycles of carbon and macronutrients (nitrogen, phosphorus, and silicon) in the ocean [1,2,3]. Excessive amounts of these metals have toxic effects, such as metabolism inhibition within algal cells [1]. After the industrial revolution, human activities have led to much emission of these bio-essential trace metals and other heavy metal pollutants into the ocean’s interior, especially in marginal seas [4,5,6]. As trace metals can serve as useful tracers and proxies for identifying sources and biogeochemical processes [7], investigating the contribution of different sources to marine trace metals is therefore essential to better understand the biogeochemical cycling of trace metals in modern oceans and to assess the impacts of human activities on marine ecosystems. To date, numerous studies on trace metals and their isotopes in dissolved and suspended particles in the ocean have been conducted globally under the framework of the international GEOTRACES program [8]. However, these studies on trace metals are mostly focused on the surface ocean and are based on instantaneous sampling. Due to sparse observations, the temporal and spatial variability of natural or anthropogenic trace metals from the surface to the deep ocean are restricted.

Mooring sediment traps can automatically and continuously collect marine sinking particles with long-term observations (months to years). Trace metal compositions in sinking particles retain valuable information to identify their sources and investigate the associated cycling processes. For example, it has been demonstrated that Al, Fe, Ti, and Th are useful indicators for mineral dust deposition [9]. In addition, Cu, Pb, Zn, and V are enriched in sediment trap samples relative to their crustal abundance in the North Pacific Western Subarctic Gyre and Sargasso Sea [10,11,12], suggesting that anthropogenic signals in trace metals can be captured by sinking particles. Via the two limited deployments of sediment traps at the SEATS station in the northern South China Sea (NSCS), it has been observed that trace metals (Co, Ni, Cu, Zn, and Cd) originating from anthropogenic aerosols can combine with sinking particles and be transported downwards to the deep ocean [13,14,15,16]. Nevertheless, how much external bioactive trace metals contribute and how they are transported from the surface to the deep water have not yet been fully elucidated.

As the largest developing country in the world, China is suffering from severe trace metal pollution as a result of urbanization and industrial development. The increasing anthropogenic emissions of trace metals and possibly subsequent increased input to the NSCS, which is adjacent to densely populated southern China, is thus an ideal location to investigate the contribution of anthropogenic sources to marine trace metals and the underlying control mechanisms. Here, time-series samples intercepted via three synchronized moored sediment traps, deployed at 1000 m, 2150 m, and 3200 m in the NSCS during June 2009–May 2010, were analyzed to quantify the mesopelagic and bathypelagic particulate trace metal fluxes. Trace metals of different origins were quantitatively assessed using a mass balance approach and then their relationships with the major components of sinking particles were examined. We aimed to quantify the contributions of different sources to bioactive trace metals in sinking particles and to better understand the role of various carriers in transporting these bioactive trace metals to the deep sea.

2. Materials and Methods

2.1. Study Area and Sample Processing

The South China Sea (SCS) is one of the largest marginal sea in the North Pacific Ocean. Due to its location in the East Asian Monsoon (EAM) region, two distinct seasonal monsoons greatly impact the primary production in the NSCS. The highest production occurs during winter, which is induced by intensive mixing and the prominent nutrient supply caused by the strong northeast monsoon and surface cooling. On the other hand, the lowest production occurs during summer, primarily due to the limited nutrient supply resulting from strong stratification with a weaker southwest monsoon [17,18,19]. In addition, the northeast monsoon can transport a significant amount of both dust and anthropogenic aerosols from East Asia to the surface layer of the NSCS in winter and spring [20,21]. Moreover, there is a certain amount of marine trade and ship traffic in our study area [22].

Three synchronized moored sediment traps (Mark 7G-21, 0.5 m² collecting area) were deployed at the SCS-N station (18.5° N, 116° E, water depth 3736 m) at approximately 1000 m, 2150 m, and 3200 m depths from 27 June 2009 to 13 May 2010 (Figure 1). The collection interval for each sample was 16 days. Twenty samples were collected at 1000 m, 2150 m, and nineteen samples were collected at 3200 m. Trapping cups (Polypropylene, Nalgene) were acid washed and then filled with a brine solution containing guarantee reagent grade 35 g L⁻¹ NaCl and 3.3 g L⁻¹ HgCl₂ before deployment [18,19]. After recovering the three sediment traps, the trapping cups were detached, sealed, and then stored at 4 °C for later analysis.

2.2. Chemical Analyses

The sediment trap samples were first passed through a 1 mm mesh nylon sieve and any remaining swimmers were removed manually. The remaining < 1 mm part was quickly divided into equal fractions using a high-precision rotary splitter (McLane WSD-10) filtered on 0.4 μm pre-weighed Nuclepore filters and dried at 40 °C for 72 h for later analysis [23].

The details of organic carbon and CaCO₃ measurements have been illustrated by Lahajnar [24]. The method of opal analyses was described in a previous study [19]. Total organic matter (OM) was derived from POC × 1.8 [25]. The relationship between these major components was described using an empirical equation [26] as follows:

Lithogenic matter flux = Total mass flux − (OM flux + CaCO₃ flux + opal flux)

2.3. Trace Metal Analyses

The sediment trap samples were analyzed for aluminum (Al) and six other bioactive trace metals, Fe, Mn, Co, Ni, Cu, and Zn, as well as phosphorus (P). The analysis was conducted using a slightly modified method described by Liao [15]. The process parameters of digestion, extraction, and dilution of sinking particle samples are shown in

Table 1. Procedure for digestion, extraction, and dilution of sinking particle samples.

Process	Solution	Volume	Temperature	Time
Predigestion	super pure HNO3-HF (1:5 v/v)	3 mL	110 °C	12 h
Dryness	/	/	110 °C	6 h
Digestion	super pure HNO3-HF (1:5 v/v)	3 mL	190 °C	48 h
Digestion	super pure 50% HCl and HNO3 (4:1 v/v)	3 mL	110 °C	6 h
Dryness	/	/	110 °C	6 h
Dryness (removing HF and HCl)	50% ultrapure HNO3	3 mL	110 °C	6 h
Extraction	50% ultrapure HNO3	3 mL	110 °C	12 h
Dilution	2% ultrapure HNO3	~9 mL	25 °C	/

.

The trace metals of Mn, Co, Ni, Cu, and Zn were measured using inductively coupled plasma–mass spectrometry (ICP–MS, Thermo Fisher, Icap-RQ). Al, Fe, and P were measured using inductively coupled plasma–optical emission spectrometry (ICP–OES, Agilent 5110). The detection limits of ICP–MS for trace metals (Mn, Co, Ni, Cu, and Zn) are typically at a low ng L⁻¹ level and the detection limits of ICP–OES for Al, Fe, and P are at a low μg L⁻¹ level. The concentrations of all the final dilution samples measured for these elements were at least one order of magnitude higher than the detection limits. The analytical precision was within 5% for all elements. The background concentration of trace metals in the trap solution was significantly lower (at least two orders of magnitude) than the total concentration of trace metals in the sinking particles. This indicates that contamination from the brine solution can be negligible.

2.4. Statistical Analysis

SigmaPlot 12.5 was used for linear regression analysis in this study. Pearson’s correlation coefficient square (R²) was used to examine correlations among element fluxes, as well as particle trace metal fluxes and major components fluxes. A significance level of p < 0.05 was applied.

3. Results

The raw elemental fluxes of P, Al, Fe, Mn, Co, Ni, Cu, and Zn at 1000 m, 2150 m, and 3200 m depths are shown in

Table 2. The raw data of the elemental fluxes (μmol m⁻² d⁻¹) in sinking particles at 1000 m.

No.	Interval Start	Interval End	P	Al	Fe	Mn	Co	Ni	Cu	Zn
1	06/27/09	07/13/09	2.36	84	22.3	0.91	0.008	0.05	0.08	0.14
2	07/13/09	07/29/09	2.36	90	23.6	1.24	0.011	0.05	0.07	0.17
3	07/29/09	08/14/09	2.84	97	24.6	1.16	0.010	0.05	0.06	0.15
4	08/14/09	08/30/09	2.61	57	46.1 *	1.00	0.008	0.06	0.10	0.33
5	08/30/09	09/15/09	1.62	35	10.3	0.50	0.004	0.02	0.03	0.15
6	09/15/09	10/01/09	1.38	45	12.1	0.76	0.006	0.03	0.05	0.24
7	10/01/09	10/17/09	1.59	46	12.3	0.78	0.006	0.03	0.04	0.10
8	10/17/09	11/02/09	2.49	84	22.9	1.04	0.009	0.05	0.05	0.20
9	11/02/09	11/18/09	7.12	356	87.7	3.75	0.038	0.16	0.16	0.40
10	11/18/09	12/04/09	8.10	532	128.7	3.81	0.042	0.14	0.12	0.37
11	12/04/09	12/20/09	4.66	200	53.0	1.86	0.019	0.07	0.07	0.18
12	12/20/09	01/05/10	4.08	253	65.7	2.45	0.025	0.09	0.09	0.22
13	01/05/10	01/21/10	6.97	116	29.3	1.33	0.012	0.05	0.05	0.15
14	01/21/10	02/06/10	3.45	91	23.9	1.17	0.010	0.04	0.05	0.12
15	02/06/10	02/22/10	5.83	224	58.5	3.01	0.026	0.11	0.12	0.23
16	02/22/10	03/10/10	4.71	171	44.6	2.29	0.019	0.08	0.10	0.26
17	03/10/10	03/26/10	1.36	67	17.6	0.77	0.007	0.03	0.03	0.11
18	03/26/10	04/11/10	7.45	606	145.2	4.27	0.052	0.16	0.15	0.41
19	04/11/10	04/27/10	4.79	336	83.3	2.94	0.031	0.12	0.12	0.34
20	04/27/10	05/13/10	4.13	231	57.4	2.40	0.024	0.09	0.10	0.29

* indicate the abnormal data.

,

Table 3. The raw data of the elemental fluxes (μmol m⁻² d⁻¹) in sinking particles at 2150 m.

No.	Interval Start	Interval End	P	Al	Fe	Mn	Co	Ni	Cu	Zn
1	06/27/09	07/13/09	2.25	117	30.4	1.88	0.016	0.06	0.09	0.33
2	07/13/09	07/29/09	2.11	119	31.0	1.93	0.016	0.06	0.10	0.19
3	07/29/09	08/14/09	2.57	139	41.7	2.35	0.019	0.07	0.12	0.21
4	08/14/09	08/30/09	1.92	117	33.6	2.31	0.019	0.06	0.10	0.16
5	08/30/09	09/15/09	1.83	109	28.3	2.15	0.018	0.06	0.09	0.15
6	09/15/09	10/01/09	1.44	84	26.7	1.72	0.014	0.05	0.08	0.13
7	10/01/09	10/17/09	1.76	84	22.7	1.69	0.014	0.04	0.07	0.13
8	10/17/09	11/02/09	0.66	39	10.4	0.74	0.006	0.02	0.03	0.10
9	11/02/09	11/18/09	4.13	274	68.9	4.31	0.038	0.11	0.17	0.31
10	11/18/09	12/04/09	5.02	355	88.1	4.04	0.038	0.13	0.16	0.29
11	12/04/09	12/20/09	6.86	460	115.8	5.59	0.054	0.17	0.21	0.45
12	12/20/09	01/05/10	5.07	422	107.2	5.00	0.048	0.15	0.19	0.36
13	01/05/10	01/21/10	3.70	251	63.8	3.15	0.029	0.09	0.13	0.28
14	01/21/10	02/06/10	3.65	226	57.4	3.18	0.027	0.10	0.13	0.35
15	02/06/10	02/22/10	4.03	253	65.5	3.60	0.031	0.10	0.15	0.27
16	02/22/10	03/10/10	3.93	304	77.8	4.06	0.036	0.11	0.16	0.28
17	03/10/10	03/26/10	3.46	292	75.2	3.95	0.034	0.10	0.16	0.32
18	03/26/10	04/11/10	5.27	484	119.6	5.46	0.054	0.14	0.20	0.44
19	04/11/10	04/27/10	3.82	360	88.7	3.52	0.036	0.11	0.14	0.52
20	04/27/10	05/13/10	2.12	172	43.3	1.87	0.019	0.06	0.09	0.25

and

Table 4. The raw data of the elemental fluxes (μmol m⁻² d⁻¹) in sinking particles at 3200 m.

No.	Interval Start	Interval End	P	Al	Fe	Mn	Co	Ni	Cu	Zn
1	06/27/09	07/13/09	-	-	-	-	-	-	-	-
2	07/13/09	07/29/09	1.92	154	38.4	2.55	0.020	0.06	0.11	0.15
3	07/29/09	08/14/09	1.83	140	35.4	2.48	0.020	0.06	0.10	0.15
4	08/14/09	08/30/09	1.88	143	37.3	2.58	0.025	0.18	0.11	0.27
5	08/30/09	09/15/09	1.84	138	34.2	2.54	0.021	0.06	0.10	0.14
6	09/15/09	10/01/09	1.91	132	32.9	2.62	0.021	0.06	0.11	0.13
7	10/01/09	10/17/09	1.68	115	28.3	2.37	0.019	0.06	0.10	0.18
8	10/17/09	11/02/09	1.56	124	30.6	2.59	0.021	0.06	0.10	0.13
9	11/02/09	11/18/09	1.70	126	33.3	2.60	0.022	0.06	0.10	0.16
10	11/18/09	12/04/09	2.35	195	49.4	4.09	0.038	0.13	0.14	0.19
11	12/04/09	12/20/09	4.32	312	77.8	4.92	0.044	0.11	0.16	0.24
12	12/20/09	01/05/10	4.14	378	93.7	4.94	0.061	0.13	0.20	0.27
13	01/05/10	01/21/10	3.78	348	86.7	4.37	0.053	0.12	0.18	0.25
14	01/21/10	02/06/10	3.74	361	93.1	4.54	0.049	0.13	0.18	0.28
15	02/06/10	02/22/10	4.00	292	73.9	4.74	0.041	0.11	0.16	0.34
16	02/22/10	03/10/10	4.25	273	69.4	4.64	0.041	0.13	0.16	0.22
17	03/10/10	03/26/10	3.59	291	74.4	4.77	0.041	0.12	0.18	0.56
18	03/26/10	04/11/10	3.16	252	64.2	4.45	0.039	0.09	0.16	0.22
19	04/11/10	04/27/10	3.68	306	76.4	4.98	0.046	0.11	0.17	0.26
20	04/27/10	05/13/10	2.15	205	50.7	2.84	0.027	0.07	0.11	0.18

, respectively. In general, the observed flux of different elements varied greatly and each element was the same order of magnitude at near depth compared to the SEATS station near our study site [13]. As expected, Al was quantitatively the most abundant trace element in sinking particles, being on average approximately four times more abundant than Fe and at least one order of magnitude higher than other trace metals. The average element fluxes were in the sequence of Al > Fe > Mn ≈ P > Zn > Ni ≈ Cu > Co. In addition, the measured bioactive trace metals displayed similar seasonal patterns, with two high fluxes observed in winter (from November 2009 to February 2010) and spring (from late March to April 2010) and the lowest fluxes presented in summer. This seasonal pattern was consistent with the trapped flux of biogenic matter (organic matter, CaCO₃, and opal) and lithogenic matter [18,19,27], which is closely tied to seasonal variations in the primary production in the SCS.

The vertical profiles of the average element fluxes are shown in Figure S1. The fluxes of P decreased with the increasing depth due to the remineralization of organic matter. Al and Fe, which are commonly assumed to be derived from lithogenic sources, showed a similar elevated flux pattern from the shallow depth to the middle depth and then remained constant at the deep depth. The other five bioactive trace metals are assumed to be driven by biological processes; however, the fluxes of Mn, Co, Ni, and Cu gradually increased with the depth and Zn displayed the highest average flux in the middle layer.

4. Discussion

4.1. Source Identification

To identify the predominant origins by which natural or anthropogenic sources dominated the trace metals in sinking particles, more comprehensively, we used three kinds of approaches via elemental correlation, the enrichment factor (EF), and principal component analysis (PCA) [28,29].

The correlations between six bioactive trace metal fluxes and Al fluxes are depicted in Figure 2, including a comparison of the reference crustal ratios and anthropogenic aerosol ratios (see Table S1). At all three trap depths, the fluxes of Fe were most strongly correlated with the fluxes of Al (R² = 0.997, p < 0.0001) and the intercept almost passed through zero. Obviously, Mn, Co, Ni, Cu, and Zn exhibited weaker linear correlations with Al than Fe and their intercepts did not pass through zero. In addition, only the proportion of Fe to Al was close to that of crustal materials, and other bioactive trace metal to Al ratios were between the reference crustal ratios and anthropogenic aerosol ratios. These results indicate that Fe in sinking particles was mainly derived from lithogenic sources, whereas the sources of Mn, Co, Ni, Cu, and Zn were probably affected by various degrees of human activities.

Generally, geochemical normalization with Al can provide a relatively unbiased interpretation of the variation in trace metals from different sources in sinking particles [13], enabling the assessment of the enrichment factor (EF) to determine if a given trace metal [M] in sinking particles is enriched relative to the crustal sources [30]. EF values of sinking particles can be calculated using the following equation, $\mathrm{EF}=\frac{{\left[\mathrm{M}\right]/\left[\mathrm{Al}\right]}_{\mathrm{particle}}}{{\left[\mathrm{M}\right]/\left[\mathrm{Al}\right]}_{\mathrm{crust}}}$ [31,32]. If the EF value is greater than 2, it is considered significantly affected by human activities. The average EF values for each bioactive trace metal at the three sampling depths, as well as the comparison with sinking particles (<160 m) in the NSCS [33], are depicted in Figure 3. In the surface water of the NSCS, the average EF values of particle trace metals Ni, Cu, and Zn are >100, where Fe, Mn, and Co are between 3.1~6.5, which are attributed to the high anthropogenic aerosol inputs [33,34]. Due to the decomposition of biogenic matter, the EF values of all six bioactive trace metals decreased in the twilight zone, especially for Ni, Cu, and Zn. In the mesopelagic and bathypelagic zone, the EF values of lithogenic Fe in sinking particles were very close to the unit (ranging from 1.1~1.5). Cu was the most enriched in the continental crust with EF values averaged 5.4 ± 2.0 and ranging from 1.9 to 14.2, followed by Zn (4.1 ± 2.7, ranging from 1.9 to 15.8) and Mn (4.1 ± 1.0, ranging from 2.0 to 5.8). Intriguingly, the enrichment of Zn gradually decreased with the depth (EF values averaged 5.3 ± 4.1, 3.8 ± 1.4, and 3.0 ± 1.0 at 1000 m, 2150 m, and 3200 m, respectively), while the enrichment of Mn gradually increased with the depth (EF values averaged 3.3 ± 0.8, 4.2 ± 1.0, and 4.8 ± 0.8 at 1000 m, 2150 m, and 3200 m, respectively). Co displayed slightly enriched (1.9 ± 0.4, ranging from 1.1 to 2.9) but followed the same enrichment pattern as Mn, as suggested by their scavenge-type trace metal in the Sargasso Sea [31]. The EF values of Ni ranged from 1.7 to 8.3, with an average of 3.1 ± 1.1.

PCA is useful for evaluating the concentration correlations and potential sources of these elements in sinking particles at the three trap depths [13,35]. The PCA results showed that the first two major components could explain 76.5, 72.6, and 55.8% of the total variance in the concentrations of trace metals in sinking particles at 1000 m, 2150 m, and 3200 m, respectively (Figure 4). Al and Fe were mainly controlled via the first component and were mainly related to lithogenic material at all three sampling depths, which agrees with the results of elemental correlations and the enrichment factors. For the second component, it appears that Cu and Zn were predominantly associated with organic matter at the three depths, except Zn at the middle layer. The correlations between P and organic matter were weakened with the depth. While Mn and Co displayed progressively reliant behavior compared to organic matter with the increasing depth, it indicated that the export of Mn and Co was regulated by the same mechanisms.

Based on the elemental correlations, EF values, and PCA results, we found that Fe in sinking particles primarily originated from lithogenic sources. On the other hand, Mn, Co, Ni, Cu, and Zn displayed different levels of enrichment. External sources of these bioactive trace metals in China’s marginal seas are mainly river discharge, aerosol deposition, and lateral transport from the continental shelf [29]. Previous studies have shown that sediment trap samples collected at the SCS-N station were unaffected by direct riverine input [17,18]. As suggested by previous studies [18,27], resuspension and lateral advection may contribute to certain external trace metals in sinking particles. However, this source is not dominant, as the proportion of lateral transport POC in relation to the vertically settled fresh marine POC is relatively small (9–16% versus 84–91%) at the same trap site. Additionally, the ratios of bioactive trace metal to Al in sediments off southwest of Taiwan (0.22, 0.20, and 0.57 for Ni, Cu, and Zn, respectively, Table S1) [36] and the NSCS shelf (0.09, 0.10, and 0.26 for Ni, Cu, and Zn, respectively, Table S1) [37] were much lower than their ratios in our sinking particles (averaged on 0.46, 0.65, and 1.46 for Ni, Cu, and Zn, respectively). Previously, anthropogenic aerosols are the major source of dissolved and particulate trace metals in the surface water of the NSCS, Western Philippine Sea, and Northwestern Pacific Ocean [29,33,34,38], which can be transported into the deep ocean by sinking particles [13,14,15]. Therefore, anthropogenic aerosols (from fossil fuel combustion, biomass burning, and industries, etc.) as extra sources can be attributed to most anthropogenic bioactive trace metals in sinking particles. Additionally, another possible anthropogenic source is the recently revealed contribution of marine transportation activities, including the influence of fuel consumption, ballast water, oil spills, and marine oil extraction on heavy metals in marine shipping areas [39,40].

4.2. Different Source Contributions of Bioactive Trace Metals in Sinking Particles

Bioactive trace metal sources in marine particles are generally divided into abiotic and biotic fractions [33,34], lithogenic and non-lithogenic (excess) fractions [31,35,41], or lithogenic, intracellular, and adsorbed fractions [13]. Nowadays, the deposition of anthropogenic aerosols are considered as an important source of bioactive trace metals (such as Cu and Zn) in sinking particles in the NSCS [14,15]. However, the formation of the authigenic particulate phase (scavenging) can also increase the bioactive trace metal (such as Mn and Co) concentrations in sinking particles [31]. And, the quantitative contributions of scavenging processes for natural and anthropogenic sources of trace metals in the global ocean remains unknown. Hence, more appropriately, we assume that bioactive trace metals in sinking particles can be divided into three major fractions: lithogenic, biogenic, and excess. Excess fractions of bioactive trace metals could originate from anthropogenic inputs, authigenic particles, and others not supported by lithogenic and biogenic materials.

Elemental ratios can provide valuable insights into the sources of particulate trace elements in the ocean as they reflect distinct elemental compositions observed in the source materials. In this study, there were strong correlations between the flux of Al and lithogenic matter at each depth (Figure S2). Thus, we assume that all Al is derived from lithogenic sources. Additionally, the POC and P fluxes exhibited a significant correlation at all three sampling depths. Moreover, the C to P ratios ranging from 99–117 in our study were very close to the Redfield ratio (106), suggesting that P can be considered a reliable indicator of biogenic components. Consequently, by applying the ratios of bioactive trace metals to Al and P in Equations (1) and (2), the contribution of the excess sources to bioactive trace metals in sinking particles can finally be quantified using the mass balance Equation (3).

F_litho = R_litho/([M]_total/[Al]_total)

(1)

F_bio = R_bio/([M]_total/[P]_total)

(2)

F_exc = 1 − F_litho − F_bio

(3)

where F_litho is the fraction of lithogenic trace metal [M]; F_bio is the fraction of organic biogenic M; F_other is the fraction of excess sources M; R_litho is the lithogenic M to Al ratio of the crust; and R_bio is the measured biogenic M to P ratio of plankton in the surface layer of the NSCS. The reference values of R_litho and R_bio are listed in Table S1.

The calculated percentages of the three major sources of bioactive metals in sinking particles at the three sampling depths are shown in

Table 5. The estimated proportion (mean ± SD %) of lithogenic (Litho.), biogenic (Bio.), and excess (Exc.) sources of bioactive trace metals in sinking particles at 1000 m, 2150 m, and 3200 m.

Trace Metal	Depth	Litho. Proportion (%)	Bio. Proportion (%)	Exc. Proportion (%)
Fe	1000 m	84 ± 4	1.2 ± 0.5	15 ± 4
	2150 m	83 ± 5	0.7 ± 0.1	16 ± 5
	3200 m	86 ± 2	0.6 ± 0.1	13 ± 2
Mn	1000 m	32 ± 9	0.2 ± 0.1	68 ± 9
	2150 m	25 ± 6	0.1 ± 0.0	75 ± 6
	3200 m	21 ± 5	0.1 ± 0.0	75 ± 17
Co	1000 m	63 ± 10	3.3 ± 1.2	34 ± 10
	2150 m	53 ± 8	1.5 ± 0.2	45 ± 8
	3200 m	45 ± 5	1.1 ± 0.1	54 ± 5
Ni	1000 m	34 ± 11	5.3 ± 2.2	61 ± 12
	2150 m	37 ± 7	3.3 ± 0.3	60 ± 7
	3200 m	35 ± 8	2.7 ± 0.6	62 ± 9
Cu	1000 m	24 ± 12	17.3 ± 7.6	59 ± 16
	2150 m	20 ± 6	8.6 ± 1.4	71 ± 7
	3200 m	19 ± 3	6.9 ± 1.1	74 ± 4
Zn	1000 m	27 ± 13	10.0 ± 4.8	63 ± 16
	2150 m	29 ± 9	6.5 ± 1.6	65 ± 10
	3200 m	37 ± 10	7.0 ± 1.8	56 ± 11

. First, the biogenic proportions of Fe, Mn, and Co in sinking particles were extremely low, while the proportions of Ni, Cu, and Zn were relatively higher. Furthermore, they behaved similarly, with the highest biogenic fraction observed at the 1000 m trap depth (Fe: 1.2%, Mn: 0.2%, Co: 3.3%, Ni: 5.3%, Cu: 17.3%, and Zn: 10.0%), followed by a decrease with the increasing depth. This can be explained by the decomposition of organic matter with the depth in sediment traps [13,42,43]. Second, among these bioactive trace metals, Fe showed the highest lithogenic fraction, followed by Co, with estimated lithogenic fractions ranging from 84 to 86% and from 45 to 63% on average in sinking particles collected at the three sampling depths. In contrast to Fe, which remained relatively uniform in the lithogenic fraction, Mn, Co, and Cu exhibited a significant decreasing pattern with the depth. This suggested that different factors control the transportation of these trace metals and Fe. Third, excess Zn was estimated to account for 63%, 65%, and 56% of the total Zn in the sinking particles at 1000 m, 2150 m, and 3200 m, respectively (Table 5), which was consistent with the estimated anthropogenic fractions of Zn with the values of 64% at both 2000 m and 3500 m at the adjacent SEATS station [15].This highlights the fact that anthropogenic Zn has emerged as the dominant source of Zn in deep water. In addition, the average fluxes and the excess proportions of Zn in the middle layer were slightly higher than those in the shallow and deep layers (Figure S1 and Table 5), suggesting that other sources of particulate Zn may originate from the scavenging of dissolved zinc or lateral transportation [15,44]. In addition to Zn, high excess proportions of Mn (68–75%), Co (34–54%), Ni (60–62%), and Cu (59–74%) were also observed in our study. The excess proportions of Mn, Co, and Cu increased gradually with the depth (Table 5), along with the trend of increasing fluxes with the depth (Figure S1). This may be related to the scavenging of redox-sensitive elements by Mn or Cu oxides [13,15,31]. Similar observations at the adjacent SEATS station indicated that elevated Mn fluxes and Mn to Al ratios at a 3500 m trap depth are attributed to the authigenic Mn oxides derived from lateral transportation [13]. As mentioned before, the high EF values (>100) of Cu and Ni are comparable with Zn in sinking particles in the surface layer of the NSCS (Figure 3); along with their relatively high biogenic proportion (Table 5) and EF values at three trap depths (Figure 3), we infer that the excess fractions of Ni and Cu may have a certain amount of anthropogenic source contributions. As previous studies in the NSCS have indicated, anthropogenic sources, particularly anthropogenic aerosols, may be dominant contributors [13,14,15,33,34].

As shown in Figure 5, in terms of the calculated three major source contributions, we found that the fluxes of six bioactive trace metals in lithogenic, biogenic, and excess fractions were significantly higher from November 2009 to May 2010 than from July to October 2010 (except excess Ni, Cu, and Zn at 1000 m). In winter and spring, the elevated fluxes of bioactive trace metal can be attributed to the enhanced advection of desert dust from Mongolian areas and the anthropogenic fine particle transport from the southeastern coast of China, driven by the northeast monsoon [20,28,45,46]. Additionally, lithogenic and anthropogenic elements are known to be scavenged faster by higher particle levels, which is driven by high primary productivity [47,48,49]. Theoretically, the wet deposition of trace metals surpassed the dry deposition by several orders of magnitude [50,51]. However, these bioactive metals were low in the sinking particles during high precipitation seasons (summer and autumn), which can be explained by the dominance of marine aerosols during the southwest monsoon and low primary productivity decreasing the organic matter ballast [49,52]. In late March to early April, another maxima of bioactive trace metal flux (particularly at 1000 m) was observed due to the occurrence of a strong Asian dust storm [19,45]. The fluxes of bioactive trace metals during the Asian dust storm were higher or comparable to that in winter. There are two possible explanations. On the one hand, after the strong Asian dust input, high and heavy lithogenic particles forming a ballast effect together with biogenic particles, which directly accelerated their sinking in the water column. On the other hand, the heavy Asian dust deposition directly provided the nutrient that stimulated the high productivity [45], where biogenic particles such as diatoms carry more lithogenic particles in aggregates, thus resulting in a high flux and reaching 50–100 m d⁻¹ sinking rates [19].

Furthermore, seasonal variations in the fluxes of Ni, Cu, and Zn from excess sources (mostly anthropogenic) were less pronounced. Sometimes, their fluxes were comparable or even higher in summer. This indicated that these excess trace metals are continuously transported from the surface to the deep ocean by sinking particles throughout the year in the NSCS. The above bioactive trace metals are crucial in various biological functions, such as nitrogen assimilation (Ni), electron transport (Cu), and carbon fixation (Zn) [2]. However, it is worth noting that these trace metals can also have toxic effects, such as the formation of reactive oxygen species due to excessive Cu levels [53]. The external input of these trace metals from anthropogenic sources could greatly alter their bioavailability or toxicity in seawater. Nonetheless, there is limited knowledge regarding their impact on marine organisms and deep ocean ecosystems, highlighting the need for further research in this area.

4.3. The Role of Various Carriers in Excess Trace Metal Transportation

The lithogenic fractions of bioactive trace metal fluxes (Fe, Mn, Co, Ni, Cu, and Zn) and lithogenic matter fluxes were highly correlated (R² = 0.947~0.984, p < 0.0001), similar to the biogenic fractions of fluxes and organic matter fluxes (R² = 0.897~0.955, p < 0.0001). However, the role of different carriers (organic matter, opal, CaCO₃, and lithogenic matter) in excess fractions of bioactive trace metal export has not yet been tested.

Adsorption of anthropogenic aerosol metals by suspended or sinking particles is highly likely to increase the excess fraction in the particles, as previous studies have suggested [13,15]. Although it is difficult to distinguish intracellular trace metals via biological uptake and extracellular trace metals via adsorption, we first conducted PCA analyses to explore potential associations between the calculated excess concentrations of bioactive trace metals and four major components in sinking particles (Figure S3). The results showed that, compared to the total concentration of these metals (Figure 4), organic matter became the first major component, accounting for 43.4% and 44.1% of the variance in the anthropogenic fraction of bioactive trace metals (Fe, Mn, Co, Ni, Cu, and Zn) at 1000 m and 2150 m, respectively. Although the first major component changed to lithogenic matter at 3200 m, the excess fractions of Mn, Co, Ni, Cu, and Zn were still more closely associated with organic matter. In addition, CaCO₃ and lithogenic matter were identified as two distinct components that can serve as ballast minerals [54].

Furthermore, we examined a straightforward correlation analysis between the excess fraction for bioactive trace metal fluxes and major component (organic matter, opal, CaCO₃, and lithogenic matter) fluxes in sinking particles at each sampling depth. As shown in

Table 6. Correlation coefficients (R²) between the fluxes of excess fractions of bioactive trace metals (Fe, Mn, Co, Ni, Cu, and Zn) and major components (organic matter, CaCO₃, opal, and lithogenic matter) in sinking particles collected at 1000 m, 2150 m, and 3200 m.

Trace Metal	Depth	Organic Matter	CaCO3	Opal	Lithogenic Matter
Fe	1000 m	0.759	0.368	0.747	0.796
	2150 m	0.659	0.497	0.687	0.735
	3200 m	0.812	0.592	0.823	0.909
Mn	1000 m	0.508	0.221	0.478	0.508
	2150 m	0.869	0.701	0.881	0.831
	3200 m	0.794	0.533	0.729	0.762
Co	1000 m	0.299	0.161	0.331	0.272
	2150 m	0.827	0.701	0.789	0.782
	3200 m	0.723	0.655	0.661	0.741
Ni	1000 m	0.387	0.155	0.322	0.279
	2150 m	0.978	0.834	0.908	0.806
	3200 m	0.582	0.385	0.490	0.555
Cu	1000 m	0.073	0.034	0.065	0.019
	2150 m	0.825	0.628	0.833	0.713
	3200 m	0.831	0.624	0.820	0.876
Zn	1000 m	0.024	0.001	<0.001	0.013
	2150 m	0.173	0.097	0.170	0.303
	3200 m	0.077	0.056	0.131	0.093

The bold numbers indicate that the Pearson’s correlation coefficient square (R²) is >0.5, with statistically significant level of p value < 0.0001.

, strong correlations were observed between excess Fe and three major components (organic matter, opal, and lithogenic matter) at all three sampling depths. Combined with the dominance of lithogenic Fe (84–86%), it is evident that the variability of Fe in sinking particles was primarily controlled via lithogenic matter. Mn, Co, and Cu exhibited very similar behavior in sinking particles in the water column, as indicated by their fluxes and enrichment patterns increasing with the depth (Figure 1, Figure 2, and Figure S1), suggesting that they have similar processes that control their distribution. As indicated in Table 6, excess Mn, Co, and Cu appear to be driven by organic matter and opal, and the ballast effect was elevated via lithogenic matter with the depth. In the shallow layer, excess Mn, Co, and Cu had the lowest correlation with the major components, especially Cu. This may be due to the extensive redox cycling that occurs in the upper water column, as described by Morel [3]. A strong association was observed between the excess Ni and organic matter (R² = 0.978, p < 0.0001), as well as opal (R² = 0.908, p < 0.0001), at a depth of 2150 m. Therefore, it can be inferred that organic matter and opal may also be essential as major carriers of excess Ni in the deep sea, which is consistent with the findings that diatoms serve as the primary biological carriers for Ni [35]. Diatoms are known for their silica-based cell walls, which can effectively biouptake, adsorb, and accumulate trace metals such as Ni and Zn [15,35]. Based on the PCA analyses, total Zn and excess Zn concentrations were closely related to organic matter (Figure 4 and Figure S3). However, evaluating the transport of excess Zn was more complicated due to the absence of any significant associations with the four major components (Table 6). Zn plays a vital role in primary production and biochemical processes, and its abundance of Zn in phytoplankton cell is comparable to that of micronutrient Fe [55]. Apart from the biological uptake, adsorption/desorption, aggregation/disaggregation of Zn, the importance of reversible scavenging in regulating the marine Zn cycle has been confirmed [15,44,56]. In addition, vertical mixing, lateral transport, and sediment resuspension and other unknown factors can also affect the transport of excess Zn from the surface to the deep water.

Finally, a schematic depiction was made to illustrate the transportation of trace metals from the surface water to the deep ocean in the NSCS (Figure 6). Anthropogenic aerosols released via the massive combustion of fossil fuels and biomass, along with ballast water discharge, oil spills, and marine oil extraction from marine transportation activities, contribute to an increased input of anthropogenic trace metals into the surface water. Some of these bioactive trace metals may have bioavailability that can be assimilated via biological uptake into the phytoplankton biomass. Additionally, natural and anthropogenic bioactive trace metals can be adsorbed, aggregated, and scavenged on biogenic particles, combined with lithogenic matter, and exported to deeper depths. The production, aggregation, sinking, disaggregation, and remineralization of biogenic particles, as well as the increase and accumulation of lithogenic particles with the depth, all regulate the transportation of excess bioactive trace metals from the surface water to the deep sea.

5. Conclusions

We investigated the different source contributions of bioactive trace metals (Fe, Mn, Co, Ni, Cu, and Zn) in sinking particles and examined the role of various carriers in the export of these trace metals in the northern South China Sea (NSCS). Except for Fe in sinking particles, which primarily originated from lithogenic sources, Mn, Co, Ni, Cu, and Zn displayed different levels of enrichment compared to their continental crustal ratios. Excess fractions of Mn (68–75%), Co (34–54%), Ni (60–62%), Cu (59–74%), and Zn (56–65%) in sinking particles were first quantified at the SCS-N station. Of which the excess fractions of Mn, Co, and Cu in sinking particles can be affected by authigenic particles. Additionally, the excess fractions of Ni, Cu, and Zn may have significant contributions from anthropogenic sources. These observations suggest that there is a significant additional source contribution of particulate bioactive trace metals, along with their transportation from the surface to the deep water. More importantly, we confirmed that biological carriers (organic matter and opal) are essential in the export of excess bioactive metals (Mn, Co, Ni, and Cu) to the deep ocean. With the intensification of human activities, the contribution of anthropogenic trace metals into the ocean’s interior should not be overlooked. More extensive observations are needed to investigate the biogeochemical cycling of excess trace metals and assess their possible effects in both the surface and deep layers.