Bioturbation coefficients and organic carbon degradation rates of deep-sea sediments in the central-eastern tropical Pacific

1. Introduction

Several processes can substantially modify the biological, chemical, and physical properties of sediments, including bioturbation, organic remineralization, and physical sediment transport processes (Aller, 1994; Steiner et al., 2016; Wheatcroft et al., 1990), affecting early diagenesis in surface sediments and sedimentary record, as well as the structure and evolution of seafloor communities (Yang and Zhou, 2004). For example, bioturbation can transport freshly deposited materials to deep sediment and result in various biogeochemical consequences. Furthermore, the bioturbation-derived mixing of materials between different aged-sediments and degradation of organic matter would also decrease the temporal resolution from sedimentary records over a wide timescale (Song et al., 2022; Smith and Schafer, 1984). Therefore, a quantitative understanding of biological mixing (i.e., bioturbation) is essential in predicting the behavior of resettled substances from mining activities. Besides, majority of the deposited organic matter may be decomposed by the biological communities that reside within the shallow sediment depths, making the bioturbation playing an important role on organic matter degradation in different spatial and timescales (Banta et al., 1995). Bioturbation can enhance degradation rates of sedimentary organic matter by stimulating priming, i.e., the mixing of freshly deposited material into deeper sediment layers (Arndt et al., 2013; Kristensen et al., 2011), consequently further affecting the net CO₂ removal from the atmosphere.

The disequilibria between two naturally occurring radionuclides, radium-226 (²²⁶Ra) and lead-210 (²¹⁰Pb) have been extensively used to examine the diagenetic processes and establish the timescales of sedimentation within the sediments (Yu et al., 2023; Nozaki et al., 1977; Soetaert et al., 1996; Suckow et al., 2001). Atmospherically derived ²¹⁰Pb (²¹⁰Pb_xs), produced from the decay of its parent nuclide, radon-222 (the daughter nuclide of ²²⁶Ra), are delivered to the waters via fallout and rapidly adsorb to sediment particles, leading to a net excess of ²¹⁰Pb (²¹⁰Pb_ex) relative to ²²⁶Ra that can be detectable for the sediment column deposited within 100 a if sediment accumulation alone controls the distribution of ²¹⁰Pb_ex. Nevertheless, the sediment mixing by bioturbation can cause the ²¹⁰Pb_ex signal extending downward below the expected zero-activity depth of ocean sediments, which makes the ²¹⁰Pb-²²⁶Ra disequilibria as a useful radiotracer pair to quantify the bioturbation-derived mixing depth (Suckow et al., 2001; Lin et al., 2021).

In the present study, two sediment cores were collected from the central-eastern tropical Pacific Ocean, followed by the application of the isotope pair ²¹⁰Pb-²²⁶Ra to estimate the bioturbation coefficients (D_B) using a steady-state diffusion model. Additionally, D_B was further combined with the organic carbon to quantify the degradation rates of organic carbon by a bio-diffusion model to understand the bioturbation-derived dynamics of organic carbon in deep Pacific sediments. Furthermore, the D_B in the study area was compared with that from other deep sea regions.

2. Materials and methods

2.1 Sampling

During the past decades, widespread deposition of manganese nodules onto the deep sediments of the Pacific and Indian oceans have received attention because of their potential as a valuable source of precious metals (Blöthe et al., 2015; Mukhopadhyay et al., 2019). The water column for tropical central-eastern Pacific Ocean region is mainly composed by six water masses, similar to those of polymetallic nodule exploration contract regions in the eastern Pacific and adjacent waters (Wang et al., 2013), including the Pacific Equatorial Water, North Pacific Central Water, California Central Water, South Pacific Central Water, Subarctic Pacific Water, and North Pacific Bottom Water, from top to bottom (Kuang et al., 2022).

During the R/V Xiangyanghong 03 Cruise in autumn 2017, two sediment cores were collected in the central Pacific Ocean by a multiple-corer, which was utilized to gather sediments without disturbance (Fig. 1 and Table 1). Water depth in the study area ranges from 4300 m to 6450 m, with an average water depth of 5350 m.

Figure  1.  Sampling locations in the central-eastern tropical Pacific.

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Table  1.  Sampling locations, water depth, bioturbation (D_B), mixing depth (L), and organic carbon degradation (OCD)

Station	Latitude	Longitude	Depth/m	DB/(cm2·a−1)	L/cm	OCD/ka−1
TRCEP-S09-MC06	9.9988°N	172.1968°W	5721	10.6	18.5	8.02
TRCEP-S07-MC04	10.0005°N	169.1996°W	4797	−	−	−
Note: − represents no data.

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After collection, they were sliced into 1 cm intervals for the upper 2 cm and 2 cm slices for remaining core. Each subsample was sealed in a clean polyethylene box, and frozen at −18℃. The sediment samples were freeze-dried and homogenized before the analysis of water contents, total organic carbon (TOC) and two radionuclides (i.e., ²¹⁰Pb and ²²⁶Ra). Water content was determined gravimetrically during freeze-drying.

Our sampling showed that surface sediment in the deep-sea basin area is clayey silt, and sand contents increases gradually from bottom to top. In the hilly region, the sediment type is clay silt, the content of sand is 1.33% to 21.2%, with an average of 11.11%. The change in sand and clay content is not obvious from bottom to top. The properties of the seafloor sediments do not change much, and they are mainly clay silty sand. The stratification of the sediments in the low and gentle hilly area is weaker than that in the deep basin area (Lin et al., 2022).

2.2 Measurement of total organic carbon

The profile of TOC was determined in two sediment cores based on Guo and Macdonald (2006) with some modification. Briefly, an approximate 1 g sample was firstly acidified for 24 h with 4 mol/L HCl solution to remove the inorganic carbon, followed by a minimum of 3 deionized water rinses. Prior to measurement with a Fisons CHN elemental analyzer, the residues were dried at 50℃ and ground for homogenization. The subsamples were analyzed in duplicate to obtain the averaged values of TOC. The precision of the TOC analysis was ±0.01% as determined by replicate analysis of standards and samples.

2.3 Determination of ²¹⁰Pb and ²²⁶Ra in sediments

The homogenized and dried samples of different sediment depths were placed into gamma counting tubes for the analysis by an ORTEC 9030 high-purity germanium well gamma detector at the decay energies of 46.5 keV for ²¹⁰Pb. The sediment samples were sealed for at least three weeks to allow secular equilibrium ingrowth of gaseous ²²²Rn from the decay of ²²⁶Ra, the parent nuclide of ²¹⁰Pb. Then the supported ²¹⁰Pb were determined from the activity of the ²¹⁴Bi from the ²²²Rn, at the decay energy of 609.3 keV. The ²¹⁰Pb_ex in sediments were determined based on the difference between total activity of ²¹⁰Pb and the supported ²¹⁰Pb (Schmidt et al., 2021).

All samples were prepared with the same geometries and counted until a counting errors of <10% was obtained. Counting efficiencies were calibrated using the different masses (1−20 g) of marine sediment standard (IAEA-385). A correction for the self-absorption of the low-energy ²¹⁰Pb gamma rays was made using the method of Cutshall et al. (1983). Activities concentrations of ²¹⁰Pb will be decay-corrected to the date of collection.

2.4 Models

2.4.1   Steady-state diffusion model

In deep-sea sediments, potential bioturbation under the low sedimentation rates (usually 1−10 cm/ka) controls the penetration of ²¹⁰Pb_ex to a depth of several centimeters. Therefore, the sediment profile of ²¹⁰Pb_ex can be used to derive the mixing by bio-diffusion from the advection-diffusion equation (Díaz-Asencio et al., 2020). Assuming a steady-state diffusion model which includes radioactive decay to describe the process of bioturbation (Cullen, 1973; Guinasso and Schink, 1975) as:

where D_B represents the bioturbation coefficient (cm²/a), x represents the depth within the sediment column (cm), A represents the activity concentration of ²¹⁰Pb_ex (Bq/kg) in the depth of x, t represents the time (a), ρ represents the bulk sediment density (g/cm³), S represents the sedimentation rate (cm/a) and $ \lambda $ represents the decay constant of ²¹⁰Pb (0.031 a⁻¹).

DeMaster and Cochran (1982) derived an equation that approximates D_B, assuming that in the mixing layer, D_B, S, and ρ are in a constant state.

The solution with the boundary conditions, assuming that A = A₀ for x = 0 and A → 0 for x → ∞, Eq. (1) is solved analytically, resulting in as following:

Since the deposition rate of deep sea is generally low (1−10 mm/ka), and the timescale of the ²¹⁰Pb-derived bioturbation is only about 100 a, the deposition of sediments can be ignored within the timescale of the tracer.

2.4.2   Bio-diffusion model

Organic matter can be transported to deeper sediment layer by bioturbation. Assuming the bulk density and sedimentation rate are constant (Canfield, 1994; Yang and Zhou, 2004), based on one-dimensional, we can use profiles of ²¹⁰Pb_ex and its relationship with TOC to derive an equation as:

where F_m denotes the metabolizable organic carbon, and k represents degradation rate of organic carbon (ka⁻¹). According to the boundary conditions: F_m = F_m0 at x = 0, and F_m → 0 at x → ∞, the F_m can be obtained as:

Based on the mass balance, the TOC can be further described as:

where F_nm is non-metabolizable organic carbon.

3. Results and discussion

3.1 TOC and water content

The sediment profiles of the TOC concentrations were presented in Fig. 2. The results showed an evident decreasing trend of TOC contents with increasing sediment depth. TOC contents in the core TRCEP-S09-MC06 ranged from 0.23% to 0.42%, averaging 0.32% ± 0.07%, high than those in seamounts of the northwestern tropical Northwest Pacific (0.14%−0.28%, Lin et al., 2021). In comparison, TOC contents in the core TRCEP-S07-MC04 were lower than TRCEP-S09-MC06, ranging from 0.18% to 0.26% with an average concentration of 0.21% ± 0.04%. Similar to the TOC, TRCEP-S09-MC06 core also showed higher water content than that in TRCEP-S07-MC04 core in general, with a decreasing from 89% to 78% with depth in TRCEP-S09-MC06 core and 79% to 60% in TRCEP-S07-MC04, respectively. Together, we can safely suggest that our two sampling stations may have different depositional environments in central-eastern tropical Pacific Ocean.

Figure  2.  Profiles of TOC and water content in two sediment cores. The dots represent the water content, and the square represents the TOC.

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3.2 Profiles of ²²⁶Ra and ²¹⁰Pb

The distribution of ²²⁶Ra and ²¹⁰Pb in two sediment cores are shown in Fig. 3. ²²⁶Ra values varied from 130 Bq/kg to 298 Bq/kg with the highest value at the 15 cm of TRCEP-S09-MC06. For the TRCEP-S07-MC04, the highest value of ²²⁶Ra was observed at 3 cm. As shown in Fig. 3, there will be not an evident change with depth for both ²²⁶Ra profiles.

Figure  3.  Profiles of specific activity of ²¹⁰Pb and ²²⁶Ra in two sediment cores.

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The ²¹⁰Pb in the sediment cores ranged from 266 Bq/kg to 1190 Bq/kg, with an average of (832 ± 251) Bq/kg. The specific activity concentrations of ²¹⁰Pb in TRCEP-S09-MC06 core consistently decreased gradually with depth, similar to the observation all throughout the ocean (Lin et al., 2021; Steiner et al., 2016; Yang et al., 2020). In contrast, increasing ²¹⁰Pb was observed between 16 cm and 21 cm of TRCEP-S07-MC04 core with the highest value at 21 cm, followed by a rapid decrease in the deeper sediment column (>21 cm). Such ²¹⁰Pb_ex variation trends, especially in TRCEP-S07-MC04 core may be a strong indicator showing the presence of bioturbation processes which introduced the freshly deposited sediments into the deeper sediment column, similar to previous observations in other oceans basins. For example, the secondary high value of ²¹⁰Pb in the sediments collected from the Peru Basin appeared at the depth of 5−20 cm, which was believed to be caused by subsurface excretion and surface feeding of animals such as echinacea (Suckow et al., 2001). The Tropical Pacific Ocean sediments showed the ²¹⁰Pb peak at subsurface sediments between 22−28 cm and 6−10 cm, attributed to Yi insect and rotate the trail of in-situ hybrid (Yang and Zhou, 2004).

The vertical distribution and highest value of the specific activity of ²¹⁰Pb were significantly different in deep-sea sediments at different stations, indicating that the deposition of ²¹⁰Pb onto the sediments was location-dependent (Suckow et al., 2001; Yang et al., 2020). In different sediment cores collected in the western North Pacific and the same stations in the eastern equatorial Pacific, there were significant differences in specific activity and preservation of ²¹⁰Pb (Thiel and Tiefsee-Umweltschutz, 2001; Yang et al., 2020). These observations show that the settlement of the deep sea sediments is spatially inhomogeneous.

Additionally, at 20 cm of the TRCEP-S07-MC04 core, a hidden manganese nodule was discovered, with a diameter of approximately 1.5 cm (Fig. 4). The specific activity of ²²⁶Ra in the manganese nodule is 2150 Bq/kg (this value was also measured by our gamma detector), similar to the observation reported by Suckow et al. (2001). The buried manganese nodule can be a source of ²²²Rn produced by the decay of ²²⁶Ra, consequently serving as the potential source for ²¹⁰Pb (Cochran and Krishnaswami, 1980). The molecular diffusion constant of radon in sediment is 1.2 × 10⁻⁵ cm²/s (Martens et al., 1980), 1−2 orders of magnitude higher than the global mean value of bioturbation coefficient (19.98 ± 42.64) cm²/a (Teal et al., 2008). Due to the short half-life of ²²²Rn (3.8 d) compared with ²¹⁰Pb, assuming the escape factor for ²²²Rn is 15% of the activity of ²²⁶Ra measured within the nodule (Suckow et al., 2001), the high value of ²¹⁰Pb in the subsurface sediment observed in the present study (Fig. 3) may be partially affected by the manganese nodule discovered in the TRCEP-S07-MC04 core. The inventory of ²¹⁰Pb from the influence of the manganese nodule was estimated to be about 20% of the total ²¹⁰Pb pool at the depth of 19 cm and 21 cm.

Figure  4.  The curve of ²¹⁰Pb activity from the one-dimensional diffusion module of ²²²Rn which is escaped from manganese nodule (sediment core TRCEP-S07-MC04).

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3.3 Vertical distribution of ²¹⁰Pb_ex

The specific activity of ²¹⁰Pb_ex in the cores ranged from 123 Bq/kg to 984 Bq/kg, with an average of (636 ± 242) Bq/kg. In the TRCEP-S09-MC06 core, the ²¹⁰Pb_ex gradually decreases with increasing depth (Fig. 5). In contrast, in the TRCEP-S07-MC04 core, the ²¹⁰Pb_ex increased gradually with the depth between surface and 23 cm and then decreased gradually with sediment depth.

Figure  5.  The relationship between the specific activity of ²¹⁰Pb_ex (Bq/kg) and depth (cm) in two sediment cores.

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Similar observation showing a maximum of ²¹⁰Pb_ex at subsurface (5−20 cm), without any indication of elevated ²²⁶Ra was also reported in other ocean regions (Smith et al., 1986; Suckow et al., 2001; Yang et al., 2020). A hybrid model “conveyor belt” or “none-in-situ mixing” was proposed to be responsible for the observed maximum value in subsurface sediments, i.e., organic matter and radionuclide-enriched surface sediments consumed by the benthos were excreted to the subsurface sediments (Smith et al., 1986). In regard to this study, as ²¹⁰Pb has a half-life of 22.3 a, the ²¹⁰Pb_ex signal can be only detectable within roughly 100 a. Considering the very low sedimentation rates (few millimeters per thousand years) in the study area, the observed ²¹⁰Pb_ex variation trend and signals as shown in Fig. 5, therefore, can strongly indicate the occurrence of bioturbation in the sediments. Nevertheless, the ²¹⁰Pb_ex signal can be also attributed to the possibility that ²²⁶Ra diffusing into deep sediments through pore water and being trapped in manganese-enriched layers (Díaz-Asencio et al., 2020; Suckow et al., 2001), like our discovered manganese nodule at 20 cm of the TRCEP-S07-MC04 core (Fig. 4). Unfortunately, the ²¹⁰Pb supported by manganese nodule-derived ²²⁶Ra cannot be quantified in the present study due to difficulties determining if other manganese nodules were present in the surrounding area of the sampling location, which requires further study in future.

3.4 Bioturbation coefficient

While evaluating the bioturbation coefficient, the possibility of ²¹⁰Pb_ex being impacted by non-local mixing and manganese nodules cannot be ignored. Due to the uncertainty of the ²¹⁰Pb possibly supported by the manganese nodule in TRCEP-S07-MC04 core, only TRCEP-S09-MC06 was included in the D_B estimation, which was calculated based on the sediment profile of ²¹⁰Pb_ex.

According to the decreasing trend of ²¹⁰Pb_ex in Fig. 5, the D_B and L at station TRCEP-S09-MC06 were estimated to be 10.6 cm²/a and 18.5 cm, respectively. This was significantly lower than the D_B of seamounts in the northwestern tropical Pacific (16.8 and 24.1 cm²/a, Lin et al., 2021; 27.1 cm²/a, Yang et al., 2020). Though, it was higher than the estimated D_B values in deep-sea sediments of the equatorial eastern Pacific (Hyeong et al., 2018), the northeast tropical Pacific, the equatorial Pacific and the western Pacific (Alperin et al., 2002; Hyeong et al., 2018; Smith et al., 1997, 1998; Yang and Zhou, 2004; Yang et al., 2011) (Table 2). This demonstrated that the study area, central-eastern tropical Pacific, had greater benthic biological activity than other regions of the Pacific Ocean.

Table  2.  ²¹⁰Pb-derived bioturbation coefficients (D_B) in the Pacific Ocean

Research area	DB/(cm2·a−1)	TOC/%	References
Northwest tropical Pacific	16.8−24.1	0.19	Lin et al., 2021
Northwest Pacific	1.01−27.1	0.26	Yang et al., 2020
Equatorial eastern Pacific	1.1−9.0	0.5	Hyeong et al., 2018
Northeast Pacific	2.1−4.4		Smith et al., 1998
Northeast tropical Pacific	0.26−2.75	0.33	Yang and Zhou, 2004
Equatorial Pacific	0.02−1.0		Smith et al., 1997
Western Pacific	1.59−8.64	0.47	Yang et al., 2011
Central-eastern tropical Pacific	10.6	0.32	this study

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Several previous studies have demonstrated that the positive correlation between the organic carbon concentration and the bioturbation intensity (Lin et al., 2021; Yang and Zhou, 2004; Yang et al., 2011). However, an opposite trend was found when comparing different regions of Pacific Ocean according to the data summarized in Table 2, showing high D_B corresponding with lower TOC. Increased food supply may lower bioturbation intensity since deposit feeders may reduce sediment reprocessing rates at times of high food availability due to homeostatic feeding (Jumars and Wheatcroft, 1989). Cammen (1979) demonstrated that the rate of ingestion varies inversely with the proportion of organic carbon in accessible sediments.

Inversely, Middelburg et al. (1997) proposed an empirical to the relationship between the bioturbation coefficient and water depth based on data from the eastern Pacific and the North Atlantic. According to the equation (D_B = 5.2 × 10^{0.762−0.004Z}), the D_B in this study area is estimated to be 0.15 cm²/a and 0.36 cm²/a, which is two orders of magnitude lower than those derived by ²¹⁰Pb_ex (Table 2). It should be mentioned that the statistical relationship between bioturbation coefficient and water depth were based on global sediment bioturbation data, which may not account for specific regional characteristics. More characteristics are required for a comparison between regions, such as bottom current, oxygen penetration into sediment, sedimentation rate, organic carbon concentration in surface sediment, and burial flow of particulate organic carbon at the sediment-water interface.

3.5 Degradation of organic carbon

Based on the reported sedimentation rate of 0.5 mm/ka in the study area (Müller and Mangini, 1980) and our observed D_B of 10.6 cm²/a, we can calculate organic carbon degradation rates using the Eq. (5) above. As shown in Fig. 6, the degradation rate of metabolizable organic carbon was estimated to be 8.02 ka⁻¹, higher than those in the central Pacific, Northeast Pacific, and central North Pacific (0.0032−4.97 ka⁻¹) (Müller and Mangini, 1980; Murray and Kuivila, 1990), suggesting that the recycling of organic matter in the sediment of central-eastern tropical Pacific Ocean was stronger than some other regions of Pacific Ocean.

Figure  6.  The content of TOC varies with depth.

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4. Conclusions

In the central-eastern tropical Pacific, radionuclide activities of ²¹⁰Pb and ²²⁶Ra were measured in the sediment cores. Significant ²¹⁰Pb_ex signals were found in both sediment cores. Based on the one-dimensional steady-state vortex diffusion model, the bioturbation coefficient of sediments was calculated (10.6 cm²/a) after removing the core impacted by the ²¹⁰Pb signal from the manganese nodule. This is lower than the global average but higher than many deep sea areas. By using a bio-diffusion model, the degradation rates of organic carbon (8.02 ka⁻¹) were calculated, which were higher than most of the Pacific. This indicated the study area has a more biological active benthic ecosystem than most deep basin areas.