Abstract
Reduced compounds dissolved in seeping fluids, such as methane and hydrogen sulfide, are the main energy sources in submarine cold seep systems, where they nourish the unique chemosynthesis-based ecosystems. Chemosymbiotic bivalves are the dominant macrofauna in many of these ecosystems and have been extensively studied due to their large biomass (hundreds of individuals per square meter), their symbiotic relationships with chemotrophic bacteria (methanotrophic bivalves: methane-oxidizing bacteria; thiotrophic bivalves: sulfur-oxidizing bacteria), and because they are unique archives of biogeochemical processes. In this chapter, we briefly introduce the advancements in seep bivalve research worldwide and then summarize the trophic modes and geographic distribution of seep bivalves in the South China Sea. Thereafter, the biogeochemical processes, such as the enzymatic strategy and energy transfer of seep bivalves, are generalized by integrating the trace elements and stable isotope data of the soft tissues and their corresponding calcareous shells of seep bivalves. Overall, we highlight the past contributions and current knowledge in this field and outline opportunities and future directions to expand this area of research.
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7.1 Introduction
Since the discovery of hydrothermal vents and cold seeps in the 1980s (Corliss et al. 1979; Paull et al. 1984), the widespread chemosynthetic ecosystems on the seabed have revolutionized our understanding of life on Earth (Fisher 1995; Dubilier et al. 2008). Within chemosynthetic environments, the high abundance of reduced compounds, such as hydrogen sulfide (H2S) and methane (CH4), serve as energy sources for carbon-fixing microbes. These microbes, in turn, form the base of the food web of dense biological communities and make significant contributions to primary production in the deep sea, deep-marine biodiversity, and marine geochemical cycles (Baker et al. 2010).
Deep-sea cold seeps are chemosynthetic ecosystems that host highly productive communities and thus enhance regional diversity on continental margins (Levin et al. 2016). Due to their ubiquity and dominance in cold seep ecosystems, chemosymbiotic bivalves—in particular bathymodiolin mussels and vesicomyid clams—have attracted the attention of researchers since the discoveries of these ecosystems. They were first investigated in the Gulf of Mexico with respect to their biogeochemical behavior (Paull et al. 1985; Childress et al. 1986; Cordes et al. 2009) and were subsequently found and studied at virtually all active cold seeps worldwide (Nankai accretionary wedge: Fiala-Médioni et al. 1993; Håkon Mosby mud volcano: Gebruk et al. 2003; pockmarks on the West African margin: Olu-Le Roy et al. 2007; Concepción methane seep area off Chile: Sellanes et al. 2008; New Zealand: Thurber et al. 2010; Marmara Sea: Ritt et al. 2012; North Atlantic and Mediterranean Sea: Duperron et al. 2013; Gulf of Cadiz: Rodrigues et al. 2013; Pacific coast of Costa Rica: Levin et al. 2015; Guaymas Basin: Portail et al. 2015; Arctic: Åström et al. 2019; Krishna-Godavari Basin: Peketi et al. 2022). After nearly 40 years of research, the understanding of the unique symbiotic relationships between seep-inhabiting bivalves and chemotrophic bacteria and the related biogeochemical processes has grown considerably (Fisher 1995; Dubilier et al. 2008; Petersen and Dubilier 2009; Lorion et al. 2013; Decker et al. 2014; Petersen et al. 2016).
Encouraging progress has also been made in discovering and understanding seep-inhabiting bivalves in the South China Sea (SCS) in the last 20 years through a large amount of investment in capital and technology. To date, three active cold seep regions (Site F, Haima and Yam) with seabed manifestations of significant gas seepage and active biological activity have been identified in the SCS, and bivalves represent the dominant macrofauna at these sites. The species, their trophic modes, and their distribution in the SCS are shown in Table 7.1 and Fig. 7.1. Among the chemosymbiotic bivalves, there are five mussel species (Bathymodiolus aduloides and Gigantidas platifrons, Hashimoto and Okutani 1994; Gigantidas securiformis, Okutani et al. 2003; Gigantidas haimaensis, Xu et al. 2019; Nypamodiolus samadiae, Lin et al. 2022), and one clam species (Archivesica marissinica, Chen et al. 2018) has been found. In addition, seven bivalve species with heterotrophic or unknown feeding strategies were found in (or near) site F and Haima seep (Han et al. 2008; Jiang et al. 2019; Ke et al. 2022).
Anatomically, chemosymbiotic bivalves are composed of soft tissue (gill, mantle, foot, siphons, etc.) and a calcareous shell, making them a unique archive for a diversity of research questions (Fig. 7.2). Soft tissue preserves information of the microenvironment that the bivalve inhabits and allows the reconstruction of biogeochemical processes, but it only provides an “instantaneous snapshot” of the brief time immediately before sampling. In contrast, the calcareous shell can provide insights into various environmental conditions during the entire lifetime of the bivalve and can potentially preserve this information for a long time and thus provide insights into evolutionary processes over geological timescales. Therefore, chemosymbiotic bivalves are excellent model organisms—their soft tissues and calcareous shell can be used to explore current and past biogeochemical processes, respectively (Wang et al. 2022a, b).
In this chapter, we compile the latest elemental and isotopic data from soft tissues and calcareous shells of diverse seep bivalves in the SCS. The trace element contents and stable isotope compositions of bivalves are outstanding indicators for evaluating their living environment, physiological functions, pathways of energy, and food sources. Together with the understanding of important biogeochemical processes of deep-sea cold seeps, we discuss the variations in geochemical composition in seep-inhabiting bivalves and provide new insights based on recent findings.
7.2 Tissue Element Compositions
Only limited studies have reported trace elements in the gill, mantle and shell of the bathymodiolin mussel G. platifrons (Wang et al. 2017; Zhou et al. 2020), systematic comparative studies (inter- and intraspecific comparison and comparison between soft tissues and shells) are still sparse. Generally, trace element contents are ranked in decreasing order, Zn > Fe > Cu > Sr > Ag > As > Al > Mn > Ba > Pb ≈ Cd > Ni > Co, and it seems that the contents of transition metal elements (e.g., Zn, Fe, Cu) in soft tissues are much higher than those in corresponding shells, indicating that bivalves may have strong physiological requirements for these elements (Fig. 7.3). Undoubtedly, through more measurements over a larger geographic area, longer timespan, and more specimens than species, the interactions among trace elements, the local environments and the physiology of bivalves may be further verified.
In contrast, the contents of rare earth elements (REEs) in seep bivalve soft tissues of the SCS have been well studied (Wang et al. 2020). The aerobic oxidation of methane is thought to be largely dependent upon the use of REEs, but to date, the effects of this process on their abundance in bacteria or organisms living in symbiosis with methanotrophs remain to be evaluated. Wang et al. (2020) selected G. platifrons (methanotroph) and B. aduloides (thiotroph) from Site F and G. haimaensis (methanotroph) and A. marissinica (thiotroph) from the Haima seep site to compare the effects of different regions and different trophic modes on the contents and patterns of REEs in seep bivalves. They showed that the soft tissues of all methanotrophic bivalves had significant lanthanum (La) enrichment, whereas such a pattern was not observed in thiotrophic bivalves (Fig. 7.4). These results demonstrate that methanotrophic bivalves prospering at methane seeps display distinctive La enrichments linked to the enzymatic activities of their symbionts and that methanotrophic bacteria efficiently fractionates REE distributions in organisms and possibly in the environment.
7.3 Tissue Isotope Compositions
It is well recognized that measuring the carbon, nitrogen, and sulfur isotope compositions of the macrofauna inhabiting cold seeps is one of the most powerful approaches to identifying their food and energy sources, as well as the determination of complex trophic interactions, including symbiosis and heterotrophy (Paull et al. 1985; Childress et al. 1986; Brooks et al. 1987; Carlier et al. 2010; Decker and Olu 2012; Demopoulos et al. 2019; Ke et al. 2022). Indeed, it is possible to distinguish consumers that assimilate carbon through chemosynthesis (more 13C- and 15N-depleted) from those that rely on photosynthetic primary production (Paull et al. 1985; Brooks et al. 1987). This is because methane is much more 13C-depleted (usually δ13CCH4 < −40‰; Whiticar 1999) than dissolved inorganic carbon (DIC) in the water column (δ13CDIC ≈ 0‰), and methane is assimilated by bacteria with only a small carbon isotopic fractionation (Alperin et al. 1988). Within cold seep areas, methane is mainly consumed in the surface sediment by anaerobic oxidation of methane (AOM) coupled with sulfate reduction and produces DIC and sulfide (Boetius et al. 2000), which generates a high microbial biomass (usually a consortium of anaerobic methanotrophic archaea and sulfate-reducing bacteria) and thus can provide a significant supply of methane-derived carbon to heterotrophic bacteria and higher-level consumers (Boetius et al. 2000). The δ13C signatures of symbiotic and heterotrophic seep-related metazoans indicate whether they preferentially rely on methanotrophically or thiotrophically derived carbon (Childress et al. 1986; Brooks et al. 1987) because the net δ13C fractionation between a consumer and its diet is small (typically < 1‰; Vander Zanden and Rasmussen 2001; McCutchan et al. 2003). Methanotrophic bacteria are usually more 13C-depleted than thiotrophic bacteria that fix DIC from the water column (Paull et al. 1985). However, δ13C values of symbiotic species that exclusively rely on thiotrophic bacteria may also be strongly modified when the DIC originates from a diversity of sources, including byproducts of methane oxidation (Lösekann et al. 2008).
Sulfur stable isotopes are useful in discriminating organic matter (OM) from the water column (by phytoplankton) or from reduced sediments (by chemosynthetic microorganisms). In general, the δ34S values of seawater sulfate are quite homogeneous at ~+21‰. Carbon fixation by phytoplankton results in only a small negative fractionation of sulfur isotopes, resulting in a narrow range in the sulfur isotope composition of oceanic particulate OM (+17‰ < δ34S < +21‰; Peterson and Fry 1987). Therefore, benthic organisms that depend exclusively on phytoplanktonic production show δ34S values with similar signatures because sulfur isotopes do not significantly fractionate between trophic levels (McCutchan et al. 2003). In contrast, dissimilatory sulfate reduction by bacteria within the sediment results in strong fractionation (−25‰ < δ34S < +5‰; Carlier et al. 2010). Consequently, organisms that assimilate these reduced compounds exhibit low δ34S values as well. To some extent, additional δ34S analyses may allow differentiation between the input of photosynthetic and chemosynthetic material for seep-related organisms (Brooks et al. 1987; MacAvoy et al. 2005).
The carbon, nitrogen, and sulfur isotopes of G. platifrons, B. aduloides and A. marissinica from cold seeps in the SCS have been investigated (Fig. 7.5; Feng et al. 2015; Zhao et al. 2020; Ke et al. 2022). According to the observations of the available data, some general patterns emerge:
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(1)
Carbon and sulfur isotopic compositions of seep bivalve soft tissues are related to their respective trophic modes. The carbon isotope values of methanotrophic bivalves (−77.6‰ to −51.2‰) are obviously lower than those of thiotrophic bivalves (−37.7‰ to −33.0‰), while the sulfur isotope values show the opposite trend (methanotrophic bivalves: +1.4‰ to +19.3‰; thiotrophic bivalves: −12.9‰ to +14.6‰).
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(2)
The characteristics of the carbon isotope signatures of different soft tissue parts of methanotrophic bivalves are consistent (δ13CMantle < δ13CGill < δ13CFoot), which has implications for the carbon transmission process in G. platifrons.
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(3)
It is suggested that different nitrogen sources are used by bivalves, in which the main nitrogen source of B. aduloides is organic nitrogen from the sediments, while G. platifrons mainly uses NH4+ (Sun et al. 2017; Wang et al. 2022a, b, c). However, it remains unclear whether different nitrogen sources are responsible for the rather stable nitrogen isotope signature of B. aduloides (+1.1‰ to +1.2‰) and the lower and highly variable nitrogen isotope signature of G. platifrons (−0.9‰ to +1.3‰). Obviously, the nitrogen isotope signature archived by seep bivalves should be further explored.
7.4 Element and Isotope Compositions of Shells
By comparison, prospecting and investigation of the calcareous shells of these bivalves lags behind that of their soft tissue. Generally, due to some inherent methodological and physiological limitations related to the shell (the record of the whole life process – years to decades of accumulation, the high degree of mixing with seawater, bulk shell sampling methods, etc.), it seems that the shell reflects some insignificant geochemical signals that inevitably blend the information of seawater and carbonate. For example, trace element concentrations ranked in decreasing order for calcareous shells of G. haimaensis and A. marissinica are Sr > Mg > Ba > Zn ≈ Mn > Cu > Ni > Li ≈ Ti > Co ≈ Zr ≈ Mo ≈ U > Th, obviously because carbonate is rich in trace elements, such as Sr, Mg and Ba (Fig. 7.3; Wang et al. 2022a). However, few studies have demonstrated that shells, similar to soft tissue, can potentially be used to reconstruct biogeochemical processes (Feng et al. 2018; Wang et al. 2020). Although the REE contents of the shells are lower than those of the corresponding soft tissues, characteristic of La enrichment is also observed in the methanotrophy-related shells (Fig. 7.4). In addition, generally consistent characteristics between the carbon, nitrogen and sulfur isotopic information contained in the shell organic matter (SOM) and its corresponding soft tissue mantle are present (Fig. 7.6). In contrast to the quickly degrading soft tissue, the bivalve shell has a high preservation potential, including its original mineralogy. Hence, the geochemical signal in the shell can be used as a fingerprint of food chains, as well as to track early evidence of microbial life and to reconstruct the chemosynthetic behavior among different types of ecosystems in the geologic past (Feng et al. 2018; Wang et al. 2020).
7.5 Summary and Perspective
Research on seep bivalves in the South China Sea (SCS) has acquired a series of profound understandings that have spurred the wave of the development of cold seeps in China in the last 20 years. Studies on the elemental geochemistry, especially rare earth elements of seep bivalves, have further verified the catalysis of light rare earth elements on the aerobic oxidation of methane and provided an excellent example for exploring the coupling (enzymatic) relationship between life activities and trace elements. At the same time, by investigating the carbon, nitrogen, and sulfur isotopes of seep bivalves, temporally and spatially integrated trophic estimates used to understand and define trophic linkages among species and communities are provided.
However, it must be admitted that our knowledge of the geochemical behavior of seep bivalves is restricted since the study of the seep bivalves of the SCS is still in the initial stage of discovery and research. The existing issues include but are not limited to the following: (1) there is a large gap in the research on different species of seep bivalves. Intensive studies on the geochemical characteristics of seep bivalves focus on G. platifrons, G. haimaensis and A. marissinica, while few studies have been conducted on other species. The trace element data of soft tissues are particularly scarce. (2) The mechanism that controls the behavior of carbon, nitrogen, and sulfur isotopes in chemosymbiotic bivalves remains understudied. In addition to the interaction between host and symbiotic bacteria, facultative filter feeding among seep bivalves remains a hard-to-define factor that may obstruct predictions of the behavior of carbon, nitrogen, and sulfur isotopes in these bivalves. (3) Due to the technical difficulties of sampling the deep sea, species of nondominant bivalves are typically found only as bycatch rather than as the result of focused and systematic sampling. Promising in this respect is the Haima cold seep as it covers a vast area, and Yam is a recently discovered seep area, allowing the discovery and research of new species of bivalves.
The exploration of seep bivalves is of great significance to both biology and geology because the combination of soft tissue and calcareous shells makes them excellent model organisms to bridge contemporary earth surface processes (present) and the sedimentary record (fossil). Future research on seep bivalves should strengthen the combination of biology and geology (especially geochemistry) and further apply this research approach to all seep macrofauna, which is expected to decode the ‘vital effect’ of symbiotic organisms and their overprint on geological records. We believe that future research on seep bivalves (and all seep macrofauna) in the South China Sea cold seeps will continue to expand our knowledge of the biological activities in this unique ecosystem, and we look forward to the advancement of knowledge in the fields of life evolution, symbiotic relationships and beyond.
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Funding was provided by the National Natural Science Foundation of China (Grant: 42106059), Shanghai Sailing Program (Grant: 21YF1416800) and Chenguang Program of Shanghai Education Development Foundation and Shanghai Municipal Education Commission (Grant: 22CGA58).
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Wang, X., Kiel, S., Feng, D. (2023). New Biogeochemical Proxies in Seep Bivalves. In: Chen, D., Feng, D. (eds) South China Sea Seeps. Springer, Singapore. https://doi.org/10.1007/978-981-99-1494-4_7
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