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All issues Volume 4 / No 2 (2025) Natl Sci Open, 4 2 (2025) 20240052 Full HTML
Open Access
Issue
Natl Sci Open
Volume 4, Number 2, 2025
Article Number 20240052
Number of page(s) 14
Section Earth and Environmental Sciences
DOI https://doi.org/10.1360/nso/20240052
Published online 16 January 2025

© The Author(s) 2025. Published by Science Press and EDP Sciences.

Licence Creative CommonsThis is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

INTRODUCTION

Blue carbon coastal ecosystems, such as vegetated mangroves, saltmarshes, unvegetated bare mudflats, and creek banks, play a critical role in regulating the global carbon cycle [1–3]. Although they constitute less than 10% of the entire ocean area, they contribute over 90% of the overall burial of organic carbon (OC) in global oceans [4]. Coastal ecosystems act as vital blue carbon sinks, sequestering atmospheric CO2 and storing both marine and terrestrial carbon in sediments for centuries to millennia [3,5]. Understanding the net carbon sequestration potential and overall carbon budget of coastal ecosystems is a key focus for sustainable development.

Dissolved organic matter (DOM) is an important substrate or product of many biogeochemical processes that influence metabolism, nutrient uptake, trace metal cycling, and microbial community structure and functionality in coastal ecosystems [2,6]. Studies have highlighted the “stability” of OC pools, particularly in mineral sediments where carbon can persist for centuries through its association with minerals [7,8]. However, the impact of benthic bioturbation on OC stability in coastal sediments remains unclear [9,10]. The stabilization and reactivity of DOM are modulated by interactions with minerals, particularly reactive iron (Fe) and manganese (Mn), which can drive the bioprocessing, transformation, transport, and stabilization of OM via the interplay of biological, chemical, and physical processes [11]. Reactive minerals can also bind organic compounds to protect DOM from microbial degradation through the formation of organic-mineral complexes [12,13]. Poorly crystalline Fe oxides are crucial for protecting DOM from mineralization in marine and terrestrial systems [14]. In the Fe oxide-OM-Mn(II) ternary system, both Mn(II) and OM can be adsorbed on the Fe oxide surfaces [15]. Under oxic conditions, Fe can exert a strong protective effect on the reactivity of DOM by promoting Fe oxide-lignin association and the accumulation of mineral-bonded organic matter through Fe(II) oxidation [16,17]. However, under reducing conditions and bioturbation, which commonly occur in blue carbon sediments, Fe reduction and crystallization, combined with the frequent physical reworking of sediments, inhibit reactive Fe binding with DOM, leading to the selective loss of DOM [18]. Similarly, with the stimulation of redox reactions, Mn(II) is oxidized and transiently combined with humic acid (HA) to form Mn(III)-HA, promoting the release of organic matter [19,20].

Benthic bioturbation can regulate OC storage in sediments by altering OM composition, enhancing greenhouse gas emissions, and pore water exchange [21–24]. The increased population sizes of arthropods and earthworms in cropland agroforestry systems positively contribute to the biological habitat and support higher sediment organic carbon content (SOC) stocks [25,26]. Fiddler crabs are widely distributed and have high population densities along global coastal wetlands [27], which significantly affects OC storage in intertidal areas [10]. For instance, the burrowing and nest-building activities of fiddler crabs increase sediment permeability, enhance the interface between the sediment and atmosphere, and promote solute exchange [28–30], facilitating the release of OC [9]. Crab burrows intensify lateral carbon exchange with tidal channels [31], increasing CO2 production and release, which ultimately affects carbon sequestration [10]. Moreover, an increase in the abundance of methanogenic communities in crab borrows has been observed, leading to higher CH4 emissions [32]. Crab bioturbation can enhance the release of Fe and Mn within sediments, resulting in elevated fluxes of these and other minerals [31,33]. This was promoted by changing the sediment redox conditions, thereby accelerating the release of DOM [34]. These changes may affect the stability of OC storage, and hence, the role of coastal ecosystems in the global carbon cycle.

To assess the effects of fiddler crab bioturbation on DOM reactivities and its implications for blue carbon sequestration, we conducted a systematic study along the Chinese coastline (Figure 1 and Figure S1). We estimated the relative effects of bioturbation on DOM compositional changes at the molecular level using Fourier transform ion cyclotron mass spectrometry (FT-ICR MS, see Section “Materials and methods”). We discuss the underlying processes of reactions between Fe-Mn minerals and DOM under bioturbation, and the influence of climate gradients on these reactions. We hypothesized that bioturbation alters the coupling of Fe-Mn minerals and DOM, potentially increasing the release of labile DOM compounds, and that this effect is more pronounced as temperature and precipitation increase. We anticipate that climate change will reduce the stability of DOM storage in coastal areas by affecting bioturbation rates.

thumbnail Figure 1

The 21 study sites along a latitudinal gradient along the Chinese coast. (a) Each study site (white circle) has 1–4 types of coastal habitats, including bare mudflats, saltmarshes, mangroves, and tidal creek banks. (b) Spatial distribution of DOM content ratio between crab burrows and sediment matrix at 21 study sites. Color gradients indicate the ratio of DOM content between crab burrows and the sediment matrix. The projection on the right shows the average variation ratio of different sites. More detailed location information is provided in Table S1.

MATERIALS AND METHODS

Sampling

In this study, all sediment samples were collected along different climatic (temperature and precipitation) gradients of the Chinese coastline, spanning more than 20 latitudinal zones, covering a wide range of environmental conditions with varying temperature and precipitation properties, such as mean annual temperature (MAT, 10–25 °C) and mean annual precipitation (MAP, 232.8–3456.0 mm) from the China Meteorological Data Service Center (https://data.cma.cn/). Specifically, we sampled 21 sites distributed across a wide geographical area on the Chinese coastline, including four representative coastal regions in China: the South China Sea Area (1–4), the East China Sea Area (5–12), the Yellow Sea Area (13, 14, and 21), and Bohai Sea Area (15–20) (Table S1) in March 2022. The 53 sampling points were located along the Chinese coastal intertidal area, including 5 mangroves, 17 saltmarshes, 19 bare mudflat, and 12 creek banks. Tubuca arcuata, Gelasimus borealis, and Austraca lacteal were the most common crab species in our study sites.

We collected samples from the crab burrow walls (crab burrow samples) and the surrounding sediment matrix (i.e., sediment matrix samples). Crab burrows were randomly selected, prioritizing fresh burrows with chimney-shaped structures. Approximately 10–30 burrow samples from each habitat were collected during the low tide. Overall, more than 1000 crab burrow samples were obtained from 53 habitats. Before sampling, the exposed chimney-shaped sediments around the burrow openings were removed because of the prolonged exposure to oxygen. Sediment samples, approximately 0.5 cm thick, were collected using a small knife by rotating around the burrow walls at a depth of 2–5 cm below the opening. Besides, an extra 5–10 cm was excavated to ensure that the positions of the sediment matrix and crab burrows were not interchanged. Sediment matrix samples were taken from a location 5 cm away from the burrow center, allowing for a direct comparison of physical and chemical chemodiversity [35]. After sampling, all samples were kept in an ice box, transported to the laboratory within 24 h, and stored in the dark at −20 °C.

Sediment and dissolved organic matter characterization

The sediment samples were lyophilized after being transported to the laboratory and stored in plastic boxes at room temperature. We analyzed the particle size distribution of the samples, SOC, total nitrogen in sediment (TNS), δ13C-SOC, and the morphological characteristics of metals (Fe and Mn) in the sediment samples. Details of the physicochemical properties of the sediments are provided in Supplementary Note 1. DOM was extracted by shaking 3 g of sediment in 60 mL Milli-Q water at 200 r/min and 20 °C for 24 h and filtering through 0.22 μm polyethersulfone membrane (Millipore Express® PLUS) [36]. The pH and electrical conductivity (EC) of the DOM samples were immediately measured using a calibrated multiparameter probe (HACH HQ440d benchtop meter). The concentrations of total carbon (TC), dissolved organic carbon (DOC), and total dissolved nitrogen of water extracts (TNW) were evaluated using a total organic carbon (TOC) analyzer (TOC-L CSH/CSN analyzer, Shimadzu, Japan). Ultraviolet-visible absorbance and fluorescence excitation-emission matrix (EEM) spectra were measured using a spectrophotometer (Horiba, Japan). The EEM data were corrected for background and inner filtering, and parallel factor analysis (PARAFAC) was used to calculate the fluorescence components [37]. The DOM water quality, spectral indices, PARAFAC calculations, and fluorescent DOM components are presented in Supplementary Note 2.

Dissolved organic matter components analysis

FT-ICR MS measurements were performed on water extractable organic matter samples. All samples were filtered and acidified to pH 2 using HCl prior to solid-phase extraction (SPE) with 200 mg Priority PolL (PPL) cartridges (Bond Elut, Agilent). Analyses were performed on a 15 T ultra-high-resolution FT-ICR MS (Bruker Daltonics, Germany) with an electrospray ionization source (ESI, Bruker Apollo II) in Shenzhen, China. The details of sample pretreatment and DOM measurement using FT-ICR MS are shown in Supplementary Note 3.

The modified aromaticity index (AImod), double-bond equivalent (DBE), nominal oxidation state of carbon (NOSC), and molecular lability boundary (%MLBL) of DOM molecules were calculated following the established methods described in previous studies [38–40]. Seven biochemical groups were defined as follows: (1) lipid-like (1.5 ≤ H/C ≤ 2.3, 0 ≤ O/C ≤ 0.2, N/C ≤ 0.04, and P/C ≤ 0.03); (2) protein-like (1.5 ≤ H/C ≤ 2.2, 0.2 ≤ O/C ≤ 0.52, 0.178 ≤ N/C ≤ 0.44, and P/C ≤ 0.06); (3) amino-sugar-like (1.5 ≤ H/C ≤ 2.2, 0.52 ≤ O/C ≤ 0.7, 0.07 ≤ N/C ≤ 0.18, and P/C ≤ 0.17); (4) carbohydrate-like (1.5 ≤ H/C ≤ 2.4, 0.7 ≤ O/C ≤ 1.1, N = 0, and P = 0); (5) condensed aromatics-like (0.5 ≤ H/C ≤ 1.25 and 0 ≤ O/C ≤ 0.25); (6) lignin-like (0.75 ≤ H/C ≤ 1.5 and 0.25 ≤ O/C ≤ 0.67); (7) tannin-like (0.53 ≤ H/C ≤ 1.5 and 0.67 ≤ O/C ≤ 0.97) [41]. The relative abundance of molecules was calculated by normalizing the signal intensities of the assigned peaks to the sum of all intensities within each sample (Figure S3).

Stability evaluation of sediment organic carbon storage

The Gibbs free energy for the half reaction of organic carbon oxidation (∆GCox0) was calculated as an indicator of the stability of DOM storage [42]. To calculate ∆GCox0, we first estimated the NOSC, per La Rowe and van Cappellen [43]. The NOSC was calculated using the following equation:

NOSC= − ( ( − Z +4 a + b − 3 c − 2 d +5 e − 2 f ) / a ) +4, (1)

where a, b, c, d, e, and f represent the number of atoms of C, H, N, O, P, and S, respectively, in a given DOC species. NOSC is the nominal oxidation state of carbon, which reflects whether microbial oxidation of organic matter is thermodynamically favorable. Z is the net charge of the species. In turn, ∆GCox0 is estimated from the empirical equation:

∆ G Cox 0 =60.3 − 28.5(NOSC). (2)

Data analysis

The soil and water extract molecular parameters did not follow a normal distribution. Thus, we used the Spearman correlation between the relative intensities of individual molecules between environmental variables and chemical properties to quantify the associations of DOM molecules with environmental variables. The analysis was performed using MATLAB MathWorks for Windows (R2023b), and van Krevelen diagrams were plotted for each variable based on Spearman correlation coefficients [39]. We adopted the approach with molecules found in at least 12 samples (> 30% DOM samples) for correlation analysis, and the dataset contained 8833 molecules in 40 soil DOM samples.

A paired sample t-test was conducted to compare the differences in the bulk, optical, and molecular characteristics of DOM between the sediment matrix and the crab burrows. Alternatively, the nonparametric Wilcoxon signed-rank test was employed if the parameters did not satisfy the assumptions of the t-test. Statistical significance was set at p < 0.05. The analysis employed paired sample t-tests and nonparametric tests to assess the relationships between the variables using SPSS 27.0. We performed structural equation model (SEM) analyses to determine the relative importance of influencing factors, such as temperature and rainfall, and the physicochemical molecular properties of DOM (i.e., NOSC, AImod, DBE, and %MLBL), both inside and outside the crab burrow. The fit of the final model was evaluated using the χ2 test and root mean square error of approximation [44]. The SEM analyses were conducted using AMOS 21.0. SEM performance was evaluated using the χ2 test (p > 0.05), comparative fit index (CFI > 0.95), and root-mean-square error of approximation (RMSEA < 0.05).

RESULTS AND DISCUSSION

Crab burrowing regulates chemodiversity of DOM

Among mangroves, saltmarshes, bare mudflats, and creek banks, only slight differences were observed across the chemical characteristics of pore water, bulk characteristics of sediment texture and DOM, and between crab burrows and the surrounding sediment matrix [35] (Figure 2 and Supplementary Note 4). These included pH, EC, sediment moisture, SOC, TNS, stable carbon isotope composition of SOC (δ13CSOC), the ratio of SOC to TNS (C/N ratio), moisture, TC, dissolved inorganic carbon (DIC), TNW, and DOC.

thumbnail Figure 2

Crab burrowing enhances the release of labile molecules. (a) The violin plots compare DOM spectroscopic characteristic. Left violins in blue represent the sediment matrix and right violins in red represent the crab burrows. Red backgrounds represent values within burrows surpassing those of the matrix, while blue backgrounds indicate the opposite results. SUVA254 (L mg C−1 m−1): specific ultraviolet absorbance at 254 nm, CDOM (m−1): chromophoric dissolved organic matter, SR: spectral slope ratio. (b) Ratio of relative abundance (R.A.) of biochemical groups in crab burrows and sediment matrix (n = 20), including tannin-like, lignin-like, protein-like, condensed aromatic-like, carbohydrate-like, and amino sugar-like. Color gradients indicate the values of these ratios between crab burrows and the sediment matrix. Solid-colored bars represent molecules present in both the matrix and burrows; shaded bars represent molecules unique to either the matrix or burrows. (c) Heat map analysis of bulk characteristics of sediment and water extracts, Fe and Mn minerals, DOM spectral characteristics, molecular characteristics, and biochemical groups in the sediment matrix and crab burrows (n = 20). Color gradients indicate the values of these characteristics’ ratios in crab burrows and sediment matrix. IDEG: degradation index, IOS: island of stability, %CRAM: relative abundance of carboxyl-rich alicyclic molecules. Complete specific descriptions of DOM spectroscopic and molecular characteristics are provided in Tale S2.

We found that fiddler crab burrowing activity greatly influenced the optical chemodiversity of DOM. The DOM concentrations derived from the fluorescence analysis in crab burrows were substantially higher than those in the sediment matrix at most study sites (Figure 2b). Particularly, in Hangzhou Bay, Zhejiang (sampling site No. 9), the DOM concentration inside the burrows was 5.8% higher than that in the matrix. Surprisingly, the DOM concentration was lower in the burrows than in the matrix in the estuaries. For example, a 27.8% lower DOM concentration in crab burrows was detected at Site 17 in Diaokou, Shandong. We propose that this may be attributed to the greater water flux in large estuaries than in other coastal zones. Under such conditions, DOM in crab burrows is more easily washed out towards the nearshore during strong infiltration [45]. The biological index (BIX) and humification index (HIX) exhibited minor differences between the crab burrows and the matrix, while it is noteworthy that the fluorescence index (FI) values within the burrows were elevated by 3.1% compared to the matrix, indicating a statistically significant difference (p < 0.05; Figure 2a). This suggests an enhancement in microbial activity due to fiddler crab bioturbation [46].

Fiddler crab burrowing activity significantly influenced the regulation of DOM optical chemodiversity by environmental variants (i.e., clay, SOC and δ13CSOC) on DOM optical chemodiversity. Clay content accounts for the majority of the variation in the chemical composition of DOM [47]. DOM is a part of sediment organic matter, and its molecular composition significantly influences the biological activity of the sediment. The fluorescence intensity at the maximum for each component was represented by Fmax (in R.U.) and Fmax/DOC ratio was calculated to indicate the abundance of various fluorescent components in DOM [48]. We discovered differing trends in the correlation between the Fmax/DOC of DOM components and sediment characteristics in burrows and the surrounding matrix (Figure S2). In the sediment matrix, the Fmax/DOC of C1, C2, and C3 showed significant negative correlations with clay content (%) (p < 0.05). In crab burrows, Fmax/DOC exhibited a significant negative correlation (p < 0.05) with δ13CSOC and was more enriched in sediments with higher clay content, particularly in C1 and C2. This suggests that the distribution of DOM in the sediment matrix is modulated by the clay content and influenced by mineral weathering processes [49], whereas in crab burrows, it is regulated predominantly by microbial processes [50].

Bioturbations affect molecular stability of dissolved organic matter by regulating mineral’s reaction

We found that fiddler crab burrowing activities greatly influenced DOM molecules but only slightly affected the contents of Fe and Mn minerals (Figure 2b and c). More than 8800 molecular formulae of DOM were detected using FT-ICR MS. Our findings indicated that fiddler crab burrowing activity significantly increased the relative abundance of unstable DOM molecules (lipid-like compounds) by 59.2% (p < 0.05; Figure 2c). Furthermore, the relative abundance of lignin-like, protein-like, and condensed aromatic-like molecules found uniquely were consistently higher in crab burrows than in the sediment matrix across mangroves, saltmarshes, bare mudflats, and creek banks (Figure 2b and Figure S3). This suggests that molecular differences in DOM are primarily caused by fiddler crab bioturbation rather than habitat type. The various fractions of Fe and Mn, including the ion-exchangeable, carbonate-bound, humic acid-bound, iron-manganese oxide-bound, and strong organic-bound fractions, showed slight differences between the crab burrows and matrix (Figure 2c).

Fiddler crab burrowing appears to regulate the coupling responses of Fe-Mn minerals and DOM, leading to decreased DOM stability. Fiddler crab bioturbation significantly influenced the interactions between clay and Fe minerals in the sediment matrix, and Fe oxides were positively correlated with clay content (p < 0.05), whereas in crab burrows, no significant correlation was observed (Figure 3e and f). These findings indicate that fiddler crab bioturbation leads to the decoupling of Fe oxides from clay, thereby weakening the protective role of clay against Fe oxides [17]. The relative abundance of labile molecules (e.g., lipid-like and protein-like) showed consistent negative relationships with Fe oxides and oxidizable Mn minerals in the sediment matrix, but these relationships were reversed in crab burrows (Figure S4). These observations suggest that during redox fluctuations in burrows, Fe(III) is reduced, releasing labile molecules [17,18], whereas Mn(II) is oxidized and transiently combined with HA to form Mn(III)-HA [20], subsequently releasing labile molecules. More recalcitrant molecules (e.g., lignin-like and tannin-like) were positively correlated with Fe oxides, oxidizable Mn minerals, and Mn-HA in crab burrows than in the matrix (Figure S4). Conversely, fewer labile molecules showed a negative correlation with δ13CSOC in the burrows than in the matrix (Figure S5). We propose that some labile molecules are immediately utilized by microbes upon release.

thumbnail Figure 3

Labile molecules are more likely to be preserved in crab burrows under climate regulation. Cascading relationships of DOM marks with environmental factors. The best-supported structural equation models showed major pathways of the influences of environmental factors on NOSC and AImod in the (a, c) sediment matrix and (b, d) crab burrows, respectively. Single-headed arrows indicate the hypothesized direction of causation, and df means degree-of-freedom. Numbers on the red (i.e., positive relationships) and blue (i.e., negative relationships) arrows indicate significant standardized path coefficients at p < 0.05, whereas dotted arrows indicate insignificant pathways. The numbers adjacent to the arrows are standardized path coefficients that reflect the effect size of the relationship. The goodness-of-fit statistics for the model are presented below. Heatmap of correlations (r) between environmental variants and different fractions of Fe and Mn minerals in (e) sediment matrix and (f) crab burrows. *, **, and *** indicate significant correlation between environmental variants and the minerals at p < 0.05, p < 0.005, and p < 0.001, respectively.

Climate gradients regulate DOM stability in crab burrows

In our conceptual framework, we found that increased climate gradients enhanced Fe and Mn redox reactions inside crab burrows. Oxidizable Fe minerals correlated more significantly with MAT and MAP in the burrows than in the matrix, while oxidizable Mn minerals exhibited the opposite trend (Figure 3e and f). Moreover, more labile molecules showed positive correlations with MAT and MAP in crab burrows than in the matrix (Figure S5). These observations suggest that Fe oxide reduction and oxidizable Mn mineral oxidation are exacerbated by increasing temperature and rainfall, enhancing the release of labile molecules because the NOSC reflects the thermodynamic stability of organic matter against microbial oxidation [51].

SEM of the environmental variants (i.e., EC, minerals, and climate gradient) showed a good fit and revealed that an increased climate gradient can weaken DOM stability in crab burrows across four different habitats: mangrove, saltmarsh, bare mudflat, and creek bank (Figure 3 and Figure S6). DOM proxies, such as NOSC, AImod, DBE, and %MLBL in the matrix, were primarily influenced by EC. However, these proxies in crab burrows were mainly dependent on climate gradients, with MAT having a direct negative effect on NOSC, AImod, and DBE and a positive effect on %MLBL. This can be explained by the release of labile molecules in crab burrows, but it becomes more difficult for microbes to utilize with increased temperatures and tends to be retained in the sediment [52,53].

Significance and implications

The stability of the DOM molecular structure ultimately influences the fate of carbon. High-energy mineral-bound molecules persist for millennia relative to low-energy unbound molecules [54]. Our results demonstrated that labile molecules (e.g., lipid-like and protein-like compounds) were negatively correlated with Fe oxides and oxidizable Mn minerals in the sediment matrix. However, these relationships were reversed in crab burrows, and lipid-like compounds were significantly more abundant than those in the sediment matrix. These results suggest that bioturbation significantly affected the molecular compositional characteristics of DOM by disrupting Fe and Mn mineral associations. Across the data set, crab burrowing activities increased the Gibbs free energy of the half-reaction of OM oxidation (∆GCox0) by 2.0% (p < 0.05; Figure 4). Especially at Site 11 in Rudong, Jiangsu, ∆GCox0 in crab burrows was 15.6% higher than that in sediment matrix. These results indicate that the thermodynamically favorable carbon decreases under fiddler crab bioturbation. The degree of ∆GCox0 difference was greatest in mangroves (2.6%), followed by bare mudflats, creek bank, and saltmarshes. Moreover, climatic factors such as temperature and rainfall significantly increased the concentration of labile molecules in crab burrows, which exhibited high thermodynamic stability against oxidation. These DOM compounds, which are easily utilized by microbes, are produced in crab burrows, and the burrow microenvironment cannot provide thermodynamic energy for microbes to utilize them [42]. Consequently, the input of labile DOM into the sea would increase with sea level rise [55], potentially disrupting ocean and offshore carbon cycling [56,57]. Thus, benthic fiddler crab bioturbation indirectly reduces the stability of OC storage.

thumbnail Figure 4

Gibbs free energy of the half reaction of organic carbon oxidation (∆GCox0) showed more unstable SOC in crab burrows than that in sediment matrix. ∆GCox0 indicates the stability of soil organic carbon. The larger the value is, the more unstable it is.

Our research suggests that fiddler crab bioturbation can significantly alter the interactions between DOM and Fe-Mn minerals, potentially reducing the stability of OC storage. Bioturbation ultimately produces biologically active DOM compounds that, once discharged, would probably be reused and mineralized because of altered environmental conditions [58]. This implies that the output of labile DOM compounds reduces the potential for blue carbon burial in the coastal zone.

Moreover, owing to habitat degradation and loss in the intertidal areas, the populations of fiddler crabs increased significantly along with the decline in top predators (e.g., birds [59]). Because crab burrowing may increase the release of DOM, the rapid increase in fiddler crabs may promote the release of blue carbon from coastal wetlands in the short term, which is a potential threat to the protection of global carbon storage [52]. Understanding how crab burrowing interacts with carbon storage can therefore provide a more effective early warning of changes in intertidal blue carbon [60], especially as human disturbance of intertidal ecosystems gradually increases and fiddler crabs explode due to the loss of natural predators.

Overall, our study concludes that fiddler crab burrowing activity has significant potential to influence biogeochemical cycling and the stability of carbon storage across coastal ecosystems (Figure 5). Specifically, our findings offer initial evidence that fiddler crab bioturbation may alter the coupling process of Fe-Mn minerals and DOM along coastal wetlands. However, a more comprehensive understanding of this intricate environmental change requires further work, including combining numerical modeling with in situ monitoring and remote sensing, to cover broader spatial (i.e., global) and temporal (i.e., seasonal) scales.

thumbnail Figure 5

Schematic summary of four key driving mechanisms showing how fiddler crab burrowing affects carbon burial through direct and indirect pathways in different habitats. Mechanism 1, mineral affinity dimmish: labile molecules and Fe-Mn minerals are released from sediment clay, followed by labile molecules that are utilized by microorganisms and become recalcitrant molecules, with Fe oxides being reduced and oxidizable Mn minerals oxidized; Mechanism 2, redox switch: frequent aerobic-anaerobic shifts in crab burrows cause continuous molecule release and oxidation; Mechanism 3, climate regulate: greater rainfall lowers NOSC in DOM. Environmental energy constraints preserve labile molecules by slowing organic matter conversion; Mechanism 4, hydraulic exchange: during hydraulic exchange, bioturbation destabilizes coastal sediment and affects the transport of sediment nutrients. For example, released DOC is partly transported offshore through burrow flushing and groundwater discharge. Some of this DOC is oxidized to CO2 and DIC, which is released into the atmosphere and ocean.

Data availability

The original data are available from corresponding authors upon reasonable request.

Acknowledgments

We are grateful to Adina Paytan and Julia Guimond for their help with the data discussion.

Funding

This work was supported by the National Natural Science Foundation of China (42177046 and 12372383), Taishan Scholars Program (tsqn202408287), Guangdong Basic and Applied Basic Research Foundation (2022A1515010572), Shenzhen Science and Technology Program (JSGG20210802153535002, 20200925174525002), and Ministry of Education of China (D20020).

Author contributions

K.X. conceptualized and designed the study; H.B.P. and his team conducted the fieldwork; Y.H., P.Z., and F. P. analyzed the physicochemical properties of sediment and porewater and conducted statistical analysis; Y.L., W.K., Y.C., J.W., Z.W., C.Z., H.L., D.H., J.W., C.D., P.W., J.C., D.M., and K.X contributed to formal data analysis and data interpretation; Y.H wrote the original draft; all authors reviewed and edited the manuscript.

Conflict of interest

The authors declare no conflict of interest.

Supplementary information

Supplementary file provided by the authors. Access here

The supporting information is available online at https://doi.org/10.1360/nso/20240052. The supporting materials are published as submitted, without typesetting or editing. The responsibility for scientific accuracy and content remains entirely with the authors.

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All Figures

thumbnail Figure 1

The 21 study sites along a latitudinal gradient along the Chinese coast. (a) Each study site (white circle) has 1–4 types of coastal habitats, including bare mudflats, saltmarshes, mangroves, and tidal creek banks. (b) Spatial distribution of DOM content ratio between crab burrows and sediment matrix at 21 study sites. Color gradients indicate the ratio of DOM content between crab burrows and the sediment matrix. The projection on the right shows the average variation ratio of different sites. More detailed location information is provided in Table S1.
In the text
thumbnail Figure 2

Crab burrowing enhances the release of labile molecules. (a) The violin plots compare DOM spectroscopic characteristic. Left violins in blue represent the sediment matrix and right violins in red represent the crab burrows. Red backgrounds represent values within burrows surpassing those of the matrix, while blue backgrounds indicate the opposite results. SUVA254 (L mg C−1 m−1): specific ultraviolet absorbance at 254 nm, CDOM (m−1): chromophoric dissolved organic matter, SR: spectral slope ratio. (b) Ratio of relative abundance (R.A.) of biochemical groups in crab burrows and sediment matrix (n = 20), including tannin-like, lignin-like, protein-like, condensed aromatic-like, carbohydrate-like, and amino sugar-like. Color gradients indicate the values of these ratios between crab burrows and the sediment matrix. Solid-colored bars represent molecules present in both the matrix and burrows; shaded bars represent molecules unique to either the matrix or burrows. (c) Heat map analysis of bulk characteristics of sediment and water extracts, Fe and Mn minerals, DOM spectral characteristics, molecular characteristics, and biochemical groups in the sediment matrix and crab burrows (n = 20). Color gradients indicate the values of these characteristics’ ratios in crab burrows and sediment matrix. IDEG: degradation index, IOS: island of stability, %CRAM: relative abundance of carboxyl-rich alicyclic molecules. Complete specific descriptions of DOM spectroscopic and molecular characteristics are provided in Tale S2.
In the text
thumbnail Figure 3

Labile molecules are more likely to be preserved in crab burrows under climate regulation. Cascading relationships of DOM marks with environmental factors. The best-supported structural equation models showed major pathways of the influences of environmental factors on NOSC and AImod in the (a, c) sediment matrix and (b, d) crab burrows, respectively. Single-headed arrows indicate the hypothesized direction of causation, and df means degree-of-freedom. Numbers on the red (i.e., positive relationships) and blue (i.e., negative relationships) arrows indicate significant standardized path coefficients at p < 0.05, whereas dotted arrows indicate insignificant pathways. The numbers adjacent to the arrows are standardized path coefficients that reflect the effect size of the relationship. The goodness-of-fit statistics for the model are presented below. Heatmap of correlations (r) between environmental variants and different fractions of Fe and Mn minerals in (e) sediment matrix and (f) crab burrows. *, **, and *** indicate significant correlation between environmental variants and the minerals at p < 0.05, p < 0.005, and p < 0.001, respectively.
In the text
thumbnail Figure 4

Gibbs free energy of the half reaction of organic carbon oxidation (∆GCox0) showed more unstable SOC in crab burrows than that in sediment matrix. ∆GCox0 indicates the stability of soil organic carbon. The larger the value is, the more unstable it is.
In the text
thumbnail Figure 5

Schematic summary of four key driving mechanisms showing how fiddler crab burrowing affects carbon burial through direct and indirect pathways in different habitats. Mechanism 1, mineral affinity dimmish: labile molecules and Fe-Mn minerals are released from sediment clay, followed by labile molecules that are utilized by microorganisms and become recalcitrant molecules, with Fe oxides being reduced and oxidizable Mn minerals oxidized; Mechanism 2, redox switch: frequent aerobic-anaerobic shifts in crab burrows cause continuous molecule release and oxidation; Mechanism 3, climate regulate: greater rainfall lowers NOSC in DOM. Environmental energy constraints preserve labile molecules by slowing organic matter conversion; Mechanism 4, hydraulic exchange: during hydraulic exchange, bioturbation destabilizes coastal sediment and affects the transport of sediment nutrients. For example, released DOC is partly transported offshore through burrow flushing and groundwater discharge. Some of this DOC is oxidized to CO2 and DIC, which is released into the atmosphere and ocean.
In the text

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