Open access peer-reviewed chapter

Geo-Biological Coupling of Authigenic Carbonate Formation and Autotrophic Faunal Colonization at Deep-Sea Methane Seeps II. Geo-Biological Landscapes

By Takeshi Naganuma

Submitted: April 24th 2018Reviewed: May 21st 2018Published: August 1st 2018

DOI: 10.5772/intechopen.78978

Downloaded: 620


Deep-sea methane seeps are typically shaped with authigenic carbonates and unique biomes depending on methane-driven and methane-derived metabolisms. Authigenic carbonates vary in δ13C values due probably to δ13C variation in the carbon sources (directly carbon dioxide and bicarbonate, and ultimately methane) which is affected by the generation and degradation (oxidation) of methane at respective methane seeps. Anaerobic oxidation of methane (AOM) by specially developed microbial consortia has significant influences on the carbonate δ13C variation as well as the production of carbon dioxide and hydrogen sulfide for chemoautotrophic biomass production. Authigenesis of carbonates and faunal colonization are thus connected. Authigenic carbonates also vary in Mg contents that seem correlated again to faunal colonization. Among the colonizers, mussels tend to colonize low δ13C carbonates, while gutless tubeworms colonize high-Mg carbonates. The types and varieties of such geo-biological landscapes of methane seeps are overviewed in this chapter. A unique feature of a high-Mg content of the rock-tubeworm conglomerates is also discussed.


  • lithotrophy
  • chemoautotrophy
  • thiotrophy
  • methanotrophy
  • stable carbon isotope
  • δ13C
  • isotope fractionation
  • Δ13C
  • calcite
  • dolomite
  • anaerobic oxidation of methane (AOM)
  • sulfate-methane transition zone (SMTZ)
  • Lamellibrachia tubeworm
  • Bathymodiolus mussel
  • Calyptogena clam

1. Introduction

Aristotle separated the world into two realms, nature and living things (originally animals), the latter having structures, processes, and functions of spontaneous formation and voluntary movements [1]. He argued the difference in the manner similar to “living organisms produce stones (e.g., calculi, shells, and other bio-mineralized materials [2]), but stones do not generate living things”. However, in the view of modern science, which has an origin in the Democritean atomism that Aristotle rejected, stones may sustain, not to say generate, life as exemplified by the biological term “lithotrophy.” Etymologically, the term was coined from the Greek words líthos and tréphō that correspond to English words of “stone” and “nourishment,” respectively. Therefore, lithotrophy is interpreted as “stone-eating,” and the corresponding organisms, that is, lithotrophs, are “stone-eaters.”

Lithotrophy or stone-eating is a figurative expression and is biologically interpreted as “living on inorganic sources.” For instance, human and animals feed on organic foods and thus are not lithotrophs (but organotrophs). Lithotrophs in this chapter are defined as the organisms that derive life-sustaining energy from redox processes of inorganic materials such as hydrogen sulfide and methane. It should be noted that methane in this argument is taken as semi-inorganic (and semi-organic) as discussed in the former chapter.

It should also be noted that the term “chemoautotrophy” takes the place of lithotrophy in this chapter, because chemoautotrophy (a.k.a., chemosynthesis) is more widely used in general and provides a clearer idea about energy sources in reference to light-driven photoautotrophy (a.k.a. photosynthesis). Autotrophy indicates the inorganic carbon source, that is, CO2, for organic (biomass) production in both photoautotrophy and chemoautotrophy (Note 1). Methane, CH4, serves as an energy source and occasionally as a carbon source via “methanotrophy,” part of which is regarded as a variety of autotrophy as explained later.

Authigenic formation of líthos (stones and rocks) at methane seeps is associated with the generation of inorganic sources that feed living organisms via chemoautotrophic and methanotrophic metabolisms. In addition, their metabolisms in turn facilitate the formation of authigenic carbonates. These rock-forming (geological) and biomass-producing (biological) processes are interwoven, and they literally, more than metaphorically, interweave to form “conglomerates” of rocks and organisms [3].

Authigenic carbonates and associated unique faunas thus represent the typical landscape of methane seeps. Methane seeps are formed by various settings as reviewed in the former chapter, and a variety of carbonates and faunas (and rock-fauna conglomerates) are formed, accordingly. This chapter provides an overview of the types of authigenic carbonates and faunas based on chemoautotrophy and methanotrophy. Profiles of a stable carbon isotope signature (δ13C) of authigenic carbonates and faunal tissues are summarized. In addition, high-magnesium (Mg) contents of the conglomerate carbonates, which are potentially associated with certain geo-biological processes, will be discussed.

2. Backgrounds for landscapes of deep-sea methane seeps

Landscapes of deep-sea methane seeps are characterized by unique and exotic biological communities based on microbial chemo(thio)autotrophic and methanotrophic biomass production, not on photosynthesis (photo-autotrophy), in the dark. Representatives of the methane seep biota are mussels, clams, and gutless tubeworms ( Figure 1 ). The landscapes are also featured by occurrences of authigenic carbonate rocks that take forms of seafloor pavements, cementations, and slabs buried in sediments ( Figure 1 ). The biological processes (biomass production, production and consumption of methane, etc.) and carbonate-forming processes are interrelated in rather a complex manner, and the interrelationships and the involved processes will be outlined from a geochemical point of view, with particular respect to stable carbon isotopes.

Figure 1.

Landscape of a methane seep at 1100 m depth, off Hatsushima Island, Sagami Bay, Central Japan. The Bathymodiolus Kenk and Wilson, 1985 mussels and Lamellibrachia Webb, 1969 tubeworms colonize the authigenic carbonate rocks. The Calyptogena Dall, 1891 clams are half-buried in the sediment to move around carbonate rocks to exploit available sulfide. Photo by JAMSTEC.

In addition to abiogenic carbonates, some organisms such as mollusks and foraminiferas produce carbonate as protective shells through the process of biomineralization. Biomineralized carbonates, particularly dolomite, are also produced by microorganisms as exemplified by Desulfovibrio brasiliensis Warthmann et al., 2005 [5], for dolomite formation or dolomitization [4, 5, 6] and Bacillus subtilus (Ehrenberg, 1835) John, 1872, possessing the etfa gene (involved in energetic electron transfer) for CaCO3 deposition [7], although it is uncertain whether they are actually involved in carbonate formation in methane seeps. Carbonate formation in methane seeps is likely facilitated by the conversion of CH4 to HCO3 , that is, oxidation of methane, which is mediated by microorganisms. Oxidation of methane is done both aerobically and anaerobically, and anaerobic oxidation of methane (AOM) coupled with sulfate reduction (sulfate respiration) produces sulfide, HS, that supports chemo(thio)autotrophic biomass production in the dark.

2.1. Stable carbon isotope deviation (δ13C) and fractionation (Δ13C)

Methane, CH4, is often geochemically characterized by the ratio of stable isotopes of 13C/12C and 2H/1H or D/H (D stands for deuterium). The ratios are generally expressed as deviations (depletion or enrichment; δ) from the reference standard ratios such as the Vienna Pee Dee Belemnite (VPDB) with the 13C/12C ratio of 0.0112372 for δ13C, and the Vienna Standard Mean Ocean Water (VSMOW) with the 2H/1H (D/H) ratio of 0.00015576 for δ2H (δD) as well as the 18O/16O ratio of 0.00200520 for δ18O. The unit of ‰ (per mil) instead of % (percent) is generally used for these deviations. For example, if a 13C/12C ratio of 0.0101135 is determined for biogenic methane, its δ13C is −100‰, as calculated as (0.0101135/0.0112372 − 1) × 1000.

These deviation parameters (δ13C, δ2H (δD) and δ18O) are regarded as the indicative of dynamics (origins, sources, processes, pathways, sinks, changes, etc.) of methane and carbonates as shown in Figure 3 of the former chapter, with careful cautions for interpretations required. For example, methane that has high δ13C and δ2H values (enriched in 13C and 2H) is generally regarded as abiotic origins (geothermal and thermogenic sources); however, the “enriched” methane may also be interpreted as “leftover” or residual of methane oxidation that removes lighter isotopes (1H and 12C) faster and leaves heavier isotopes (2H and 13C) behind, or isotope fractionation (discrimination), resulting in the isotopically “enriched” (heavy) residual methane, as discussed later.

The product of methane oxidation (carbon dioxide, CO2) and the derived carbonate rock (CaCO3) contain no hydrogen isotopes but stable oxygen isotopes, 16O and 18O, of geochemical interest. The deviation (depletion or enrichment) parameter δ18O of carbonates is indicative of oxygen dynamics (origins, sources, processes, pathways, sinks, etc.) but is more readily influenced by temperature, fluid inclusion, diagenesis, and so on, than δ13C [8]. Therefore, this chapter deals mainly with δ13C that may serve as a “signature” of carbon dynamics as depicted in Figure 2 and summarized in Table 1 , and fractionation parameters (Δ13C) in the processes and pathways of carbon dynamics (focusing on methane dynamics) is also discussed later and summarized in Table 2 .

Figure 2.

An illustrated general view of carbon dynamics with reference to the processes occurring at a methane seep. Numbers in circles from 1 to 12 correspond to the numbers in Tables 2 and 3 .

Carbon speciesFormδ13C (‰)Reference
1CO2Gas (atmospheric)-8.00[9]
2DICca. 90% HCO3 0.00[9]; Bjerrum plot [13] Figure 1.1.2, p.5
3Organic CPhytoplankton biomass-22.0[9]
4Organic CSedimentary-27.0 to -22.0
-30.0 to -22.0
-80.0 to -47.0
In general [9]
Methane seeps [23, 24, 26, 144]
Brine seep at Florida Escarpment [27, 28]
5CO2Interstitial water-50.0 to -5.00 (DIC)
-38.0 to +11.0 (DIC) -21.0 to +1.00 (CO2)
-27.5 (CO2)
[25, 40, 145]
6CH4Sedimentary-100.0 to -40
-101.3 to -27.2
In general [32]
[23, 26, 31, 33]
7post-AOM CO2CH4-derived (oxidized)Not found
8CaCO3Authigenic carbonate-60.0 to +26.0[50, 56]
9post-AOM CH4Residual (unoxidized)Possibly -27.2Eel River Basin [33]
Soft tissue-55.0 to -18.0[23, 31, 41–48]
Tube (chitin + protein)-28.1 to -19.9[24, 41–44]
Soft tissue-76.0 to -36.4[27, 31, 49, 146, 147]
Shell (CaCO3)-6.80 to -2.60[27, 147]
Soft tissue-69.2 to -32.5[23, 43, 44, 146]
Shell (CaCO3)-2.00 to +0.35[23, 43, 144, 148, 149]

Table 1.

Stable carbon isotope ratio deviation, δ13C (‰), of different carbon species and forms involved in the carbon dynamics associated with methane seepage.

ProcessCarbon isotope fractionation processΔ13C (‰)Reference
1 → 2Air-to-sea transfer of CO2−2.00[12]
2 → 1(Sea-to-air transfer of CO2)(−10.0)[12]
2Hydration of CO2 (13C-enrichment in HCO3 )+8.00[14]
2 → 3HCO3 to CO2 by carbonic anhydrase+10.0[15]
2 → 3Photoautotrophy (photosynthesis in seawater)−29.0 to −11.0[16, 17, 18, 19]
3 → 4Diagenesis (shallow burial)−4.00 to −5.00[22, 150]
Diagenesis (deep burial)few[150]
4 → 5Anaerobic oxidation (organic C to CO2)Not found
4 → 6Methanogenesis (organic C to CH4)−61.5 to −31.1
−83.0 to −72.0
Peatland [29]
From methanol [30]
6 → 7AOM−29.00With nitrate (not sulfate) [36]
7 → 8Carbonate authigenesis (from CO2 or DIC)Almost 0
+0.08, +19.44
In general [9]
Certain seep cases [28]
7 → 10Chemoautotrophy−33.0 to −24.0
−11.0 to −10.0
Calvin-Benson cycle [151]
Reductive TCA cycle [152, 153]
Biomineralization (shell formation)A few; +10.0To DIC; to food [154]

Table 2.

Stable carbon isotope fractionation, Δ13C (‰), during geo-biological processes of carbon dynamics associated with methane seepage.

2.1.1. δ13C values before and after methanogenesis

Taking atmospheric CO2 as the starting material of methanogenesis, its δ13C value is currently estimated at about −8‰ ( Table 1 ) [9] with an estimate of a decrease rate of 0.05–0.06‰ year−1 [10], possibly due to the input of lighter carbon (12C) into atmosphere by artificial fossil fuel combustion, that is, the so-called “Suess effect” [11]. Air-to-seawater transport prefers lighter 12CO2 to heavier 13CO2 and thus decreases its δ13C by 2‰ (Δ13C of −2‰, Table 2 ) [12]. Part of CO2 in seawater will be hydrated toward a chemical equilibrium of CO2-H2CO3-HCO3 -CO3 2− (virtually CO2-HCO3 -CO3 2−), and these are collectively termed “dissolved inorganic carbon” (ΣDIC or simply “DIC”). Among DIC, HCO3 is the predominant ion form at seawater pH of 8.00 [13]. Fractionation between 12C and 13C also occurs during hydration of CO2 into HCO3 , back-conversion (by carbonic anhydrase) from HCO3 to photosynthetically available CO2, and photosynthesis mainly by phytoplankton that assimilate CO2 via C3 pathway (Calvin-Benson cycle, Table 2 ) [14, 15, 16, 17, 18, 19]. After all fractionations together, δ13C of eventually (photosynthetically) produced biomass is generally taken as −22.0‰ [9].

About 0.50% of the photosynthetically produced organic matter is buried in the sediment [20], where the process is often termed as “biological pump” shown in Figure 3 [21]. The δ13C values of the “biologically pumped” sedimentary organic matter decreases from −22.0‰ in shallow (fresh) to −27.0‰ in deep (old) layers, due to diagenetic fractionation [22]. Almost the same δ13C values, −22.0 to −30.0‰, of sedimentary organic matter from methane seepstwere reported [23, 24, 25, 26]. However, very depleted δ13C values, as low as −47.0 to −80.0‰, of sedimentary organic matter were also reported from the methane seep at the base of Florida Escarpment in the Gulf of Mexico [27, 28], which may be associated with “brine” seepage from very old organics or organics of non-photosynthetic origins.

Figure 3.

A schematized view of δ13C variability from atmospheric CO2 to authigenic carbonate and autotrophic fauna. The δ13C values are taken from Table 2 .

Strong fractionation occurs during methanogenesis, for example, as strong as Δ13C of >−60.0‰ in a Finnish peatland [29] and >80‰ from methanol in the laboratory [30]. Therefore, methane generated from sedimentary organic matter often shows depleted δ13C values, as low as −40.0 to −100‰ [26, 31, 32, 33]. Care should be taken to such cases that even biogenic methane may be enriched (having high δ13C values) due to microbial oxidation as described subsequently and thus mistakenly regarded as abiogenic (thermogenic) methane [34].

2.1.2. δ13C values after anaerobic oxidation of methane

In methane oxidation, heavier methane (13CH4) is less preferably oxidized, and therefore δ13C of the resultant CO2 is depleted by 5.00 to 30.0‰, that is, Δ13C of CH4 → CO2 is generally −5.00 to −30.0‰ [34]. A decrease in δ13C, or Δ13C, during aerobic microbial methane oxidation is reported to be −15.0 to −30.0‰ [35]. AOM with nitrate (not sulfate) is reported to result in Δ13C of about −30.0‰ [36]. Although Δ13C of “AOM with sulfate” has not been determined, it would not be too far from these fractionation values.

Theoretically, δ13C values of the resultant DIC forms (CO2, HCO3 , and CO3 2−) after AOM are depleted and actually determined to be −41.0‰ for DIC (virtually HCO3 ) in interstitial water, compared with δ13C −24.0‰ of sedimentary organic matter [25]. It should be remembered that Δ13C of CO2 → HCO3 is about +8.00‰ [14] ( Table 2 ), leading to a generally accepted idea and the fact that δ13C of DIC in non-seep, non-vent seawater is −2.00‰ or roughly 0‰. Returning to seep-methane-derived DIC, δ13C −41.0‰ of DIC would possibly correspond to δ13C −49.0‰ of CO2. However, such a theoretical view is often challenged by reality. An example of sequential δ13C values from sedimentary organic matter (−22.0%) and biogenic methane (−68.0‰) to CO2 (−20.0‰ to +1.00‰) and DIC (−38.0 to +11.0‰) [26] is tough to be elucidated.

2.1.3. δ13C values of authigenic carbonates and autotrophic faunas

Generally, fractionation in δ13C, that is, Δ13C, from DIC to carbonates is regarded to be zero [9]. Therefore, authigenic carbonates in methane seeps should have depleted δ13C values, as authigenesis starts with oxidation of depleted methane and proceeds with the resultant depleted CO2, as typically shown by the δ13C values of around −50‰ in the matrices, nodules, and cements of authigenic seep carbonates [37, 38, 39]. However, again, theories are challenged by unexpectedly high δ13C values ( Figure 3 ), for example, as high as +16 and +24‰ in carbonates of the Eel River Basin seeps [37, 40]. The involvement of ordinary (non-seep, non-vent) DIC and “leftover” DIC that had not been incorporated into earlier carbonate authigenesis (therefore enriched), as well as “re-worked” DIC that had been generated from leftover (enriched) CH4, is imaginable.

The seep methane and derived CO2 after AOM will also be incorporated into faunal biomass via thioautotrophic or methanotrophic biomass production by symbiotic bacteria, respectively. As the source methane and CO2 are depleted in δ13C, the biomass δ13C should be depleted accordingly. The observed δ13C values in soft tissue of the gutless tubeworms are within the range from −55.0 to −18.0‰ [23, 31, 41, 42, 43, 44, 45, 46, 47, 48]. The δ13C values of tubeworm soft tissue are relatively higher (enriched) compared with those in the soft tissue of mussels and clams inhabiting the same seeps ( Table 1 ; Figure 3 ) [46, 47, 49, 50], which may be related to the possible dual CO2-fixation pathways (C3 pathway and rTCA cycle, Table 3 ) in seep tubeworms as predicted for the endosymbiont of the vent tubeworm Riftia pachyptila Jones, 1981, by metaproteomics [51]. Hard tissues such as shells of mussels and clams show generally higher δ13C values than those in soft tissues, some of which are close to that of ordinary DIC ( Table 1 ; Figure 3 ).

Common nameFunctional nameAutotrophyΔ13C from DIC (‰)Reference
Calvin-Benson cycleC3; Reductive pentose phosphate cyclePhoto (O/A), Chemo, Methanol−33.0 to −24.0[151]
Hatch-Slack pathwayC4 carbon fixationPhoto (O)−16.0 to −10.0[151]
CAM pathwayCrassulacean acid metabolism pathwayPhoto (O)−20.0 to −10.0[151]
Reverse Krebs cycleReverse tricarboxylic acid (rTCA) cyclePhoto (A), Chemo−11.4, −10.0[152, 153]
Wood-Ljungdahl pathwayReductive acetyl CoA pathwayChemo (Methanogenesis)−36.0[152]
3-Hydroxypropionate pathwayPhoto (A), Chemo−14.0 + 3[155, 156]
3-Hydroxypropionate/4-hydroxybutyrate cycleChemo+2.50[157]
Dicarboxylate/4-hydroxybutyrate cycleChemoNot found

Table 3.

Pathways and fractionation factors, Δ13C (‰), of autotrophic CO2 assimilation.

Photo, oxygenic (O), and anoxygenic (A) photosynthesis or photoautotrophy; Chemo, chemoautotrophy; and, Methano, methanotrophy.

3. Authigenic carbonate rocks

Authigenic carbonates have recently been recognized as an important “carbon sink” in the global carbon cycling next to marine carbonates and organic matters [52], and the authigenesis occurs mainly at methane seeps via anaerobic oxidation of methane (AOM). In other words, methane seeps are often accompanied by authigenic carbonate rocks, that is, carbonate rocks that are formed in situ (autochthonously) in the seabed of methane seeps. The process generates structurally and compositionally multi-staged carbonates that are explained by not simply geochemical but biogeochemical or even microbial involvements [53]. The process may be accelerated due possibly to microbial involvements, as shown by “fresh” ages of authigenic carbonates, as fresh as 195 years old to almost zero for the carbonates exposed on the shelf slope of the Gulf of Mexico [126]; otherwise, from 53,400 to 1700 years old (53.4–1.70 kiloyears ago, ka) in the Gulf of Mexico, 45.5–3.00 ka in the Cong Fan, and 1.60–1.10 ka in the Black Sea [54], as well as 6.40–0.80 ka in the Hydrate Ridge [55].

A simplified mechanism of carbonate rock formation, or authigenesis, is as follows: methane is oxidized (mainly anaerobically with sulfate in the sediment) to generate DIC (CO2-HCO3 -CO3 2−), which will react with Ca2+ and Mg2+ to precipitate Ca(Mg)CO3. The precipitates will grow into aggregates and conglomerates of visible sizes. The real processes are not that simple [56], and they often take the forms of slabs in the sediment and pavements on the sediment, as well as half-buried aggregates with wide-ranged δ13C values. Modes of carbonate occurrence are regarded as affected not only by microorganisms but also by carbonate-dwelling macro-fauna such as tubeworms and mussels [57].

Gutless tubeworms are occasionally incorporated in aggregates ( Figure 1 ), as they require physically hard substrates for settlement and chemically aerobic-anaerobic boundaries, at which carbonates are exactly deposited though anaerobic oxidation of methane (AOM) with sulfate. Sulfide, an AOM byproduct, is aerobically oxidized by symbiotic bacteria (of the host tubeworms) with O2 to obtain metabolic energy for thioautotrophic chemosynthesis; the symbionts are localized inside of the host cells and are termed “endosymbionts.” The gutless tubeworms, therefore, colonize the hard substrates that lay in the zone where sulfide and O2 coexist, that is, exactly the zone of carbonate deposition, almost overlapping the sulfate–methane transition zone (SMTZ).

Mussels that harbor thioautotrophic and/or methanotrophic symbiotic bacteria are epibenthic and colonize the carbonate rocks that extrude the sediment for settlement ( Figure 1 ). By contrast, clams depending on bacterial thioautotrophy are semi-endobenthic and live half-buried in the sediment between and around carbonate rocks ( Figure 1 ).

Types of authigenic carbonate rocks are generally grouped into calcites (as well as aragonites) and dolomites. Calcite is further divided into high- and low-Mg calcite according to their Mg contents. Interrelations between carbonate rock types and seep faunal types, that is, between calcites-dolomites and mussels-clams-tubeworms, are hypothesized as discussed later.

Extreme 13C depletion is seen in the authigenic carbonates, when they are formed from depleted DIC (CO2-HCO3 -CO3 2−) via AOM against biogenic-depleted methane having δ13C values as low as −125‰ [58]. On the other hand, enriched DIC is derived from oxidation (probably aerobic oxidation after AOM) of residual 13C-enriched methane and yields 13C-enriched carbonates accordingly. Therefore, the δ13C ranges of authigenic carbonates are relatively greater than those of seep mussels, clams, tubeworms, and so on.

3.1. Authigenic calcite and aragonite

Among the carbonates, calcite/aragonite and dolomite are often seen in the methane seep environs. Calcite and aragonite are the carbonate polymorphs used in many marine organisms (mollusks, brachiopods, foraminiferans, corals, etc.); they have the same chemical formula (CaCO3) but are different in crystal structures [59]. Aragonite is about 1.50 times as soluble (unstable) as calcite in seawater. Calcite that has lower contents of impurity magnesium, Mg, is more stable than high-Mg calcite. Therefore, the stability order on the deep seafloor is generally low-Mg calcite, high-Mg calcite, and aragonite.

Despite the stability next to low-Mg calcite, high-Mg calcite is often seen in the methane seep environs, with occasional association with tubeworm settlement. By contrast, low-Mg calcite is associated with mussel colonization. The formation and occurrence of less stable high-Mg calcite has not yet been fully elucidated. It may be associated with the attachment and growth of colonies of tubeworms and will probably provide a platform to investigate mineral-animal (and bacteria) interaction from a geo-biological point of view.

3.2. Authigenic dolomites

Dolomite, CaMg(CO3)2 in an ideal chemical formula, is formed by replacing calcium ions of calcite with magnesium ions. Or, high-Mg calcite may be regarded as an intermediate form of dolomitization. Once there was a paradox about dolomitization at low temperatures, that is, at physiological temperatures, it was solved by the laboratory experiment using sulfur-reducing (sulfate-respiring) bacteria [4, 5, 6].

Authigenic dolomite in methane seeps has rarely been studied, and an example from the naturally exhumed fossil seep in Greece showed depleted δ13C values as low (light, depleted) as −8.00 to −29.0‰, maybe indicative of dolomite formation at the AOM zone in the sediment [60]. Authigenic dolomite in drill-cores from the oil fields in the Santa Barbara Basin, off California, showed δ13C values of −16.0 to +9.00‰; lighter values are also indicative of dolomite formation in the relatively shallower zone of AOM with sulfate reduction, while heavier values may come from the relatively deeper zone of methanogenesis [61].

4. Autotrophic faunas: Tubeworms, mussels, and clams

Methane seeps and hydrothermal vents, as well as organic falls such as whale carcasses, are located not too far from each other, particularly along the Pan-Pacific “Ring of Fire.” Similarities in taxonomic structures and energetic metabolisms (including chemoautotrophy and methanotrophy) between seep and vent fauna have been studied. While the importance of the β-diversity, that is, site-specific diversity, among the seeps and vents worldwide has been pointed out [62], faunal assemblages in the semi-enclosed Guaymas Basin in the Gulf of California (six seeps and four vents without topo-/geographic barriers) share species compositions [63]. In the same but a greater way, the ring-of-fire-type array of seeps and back-arc basin vents in the active margins (convergent margins) contribute to biogeographic connectivity of vent and seep faunas but does not support the “stepping stone” hypothesis by whale carcasses [64].

The gutless tubeworms that represent the exotic seep/vent faunas had already been known (but only sporadically sampled) since the beginning of the twentieth century, before the massive colonies were discovered in association with deep-sea volcanism at the Galápagos Rift in 1977 [65]. It took 4 years to propose that the gutless tubeworms (polychaetes) depend for their nutrition on sulfide−/sulfur-oxidizing chemoautotrophic (thiotrophic or thioautotrophic) biomass production by endosymbiotic bacteria in their specialized sac-like tissue, trophosome [66]. The trophosome is a natural “culture vessel” of, for example, not-yet-cultured thiotrophic gamma-proteobacterial Candidatus Endoriftia persephone in the case of the giant vent tubeworm R. pachyptila Jones, 1981 [67], and has still been enthusiastically investigated from not only biological but also biomedical and biotechnological points of view [68].

It also took 3–4 years after the first discovery of methane seeps in the Gulf of Mexico [69] for scientists to reveal that seep mussels depend not on thiotrophic but on methanotrophic endosymbionts in gills [70, 71]. In 1987, methanotrophic symbiosis was also found in a non-vent, non-seep gutless tubeworm (Siboglinum poseidoni Flügel and Langhof, 1983 from polychaetes) from the sediment of the central Skagerrak strait [72, 73] and some other vent/seep mussel species, but not for clams [74]. While many bivalve and gastropod mollusks have chemo−/methanotrophic symbionts [75], this chapter focuses on bivalve mussels (Bathymodiolus Kenk and Wilson, 1985) and clams (Calyptogena Dall, 1891) from seep (and vent) habitats.

Symbiosis with more than one symbiotic species in one host, which is dual or multiple symbiosis, is known for gutless tubeworms; an example is the vent-dwelling tubeworm that hosts multiple thiotrophic species as endosymbionts [76]. In addition, dual symbiosis with both thio- and methanotrophic endosymbionts has been known for the seep mussels (Bathymodiolus spp.) in, for example, the Gulf of Mexico [77] and off-Congo passive margins [78], as well as other invertebrates (mostly gutless oligochaetes) dwelling non-vent, non-seep habitats (Note 2).

In addition to thiotrophy and methanotrophy, in 2011, hydrogenotrophy (chemoautotrophy based on hydrogen oxidation) appeared as the third way of a vent mussel (and possibly for seep mussels) [79].

4.1. Thiotrophy and methanotrophy

Photosynthesis and chemoautotrophy differ in energetic processes but share the CO2-fixing pathways, for example, the best-known Calvin-Benson cycle (reductive pentose phosphate cycle). Currently, eight autotrophic CO2-fixing pathways, including Calvin-Benson cycle, are known for life even in the dark chemoautotrophy ( Table 3 ) [80]. Dual pathways are widely known in chemoautotrophy-based macro-organisms, such as siboglinid (formerly known as vestimentiferan and pogonophoran) tubeworms, of hydrothermal vents and methane seeps [48].

In addition to a variety of CO2-fixation pathways, a battery of energetic pathways with diverse reductants and oxidants (electron donors and acceptors) is also known for chemoautotrophy [81, 82]. The most representative one in the methane seeps is the oxidation of sulfide. If chemoautotrophy is based on sulfide oxidation, it is correspondingly termed “thiotrophy” or “thioautotrophy.” While aerobic oxidation of sulfide is most common, anaerobic oxidation of sulfide with nitrate, HS + NO3 → HSO4  + N2 (Note 3), (nitrate reduction, nitrate respiration, or denitrification), is possible, although its occurrence in methane seeps is not necessarily evident.

Both aerobic and anaerobic oxidation of H2 can also provide an energetic basis for chemoautotrophy. Aerobic oxidation of H2 with O2 has recently been recognized as widespread among the hydrothermal vent chemoautotrophy [79, 83]. H2 is also oxidized anaerobically with CO2, which corresponds to the autotrophic CO2 respiration, or autotrophic hydrogenotrophic methanogenesis, and represented by the thermophilic species of Methanothermobacter thermoflexus (Kotelnikova et al. 1994) Boone 2002 and M. thermautotrophicus (Zeikus and Wolfe 1972) Wasserfallen et al. 2000. However, in a non-thermophilic environment such as artificial anaerobic digesters, non-autotrophic CO2 respirers dominate the microflora [84], which gives an implication for considering CO2 respirers in the “cold” methane seeps.

Methanotrophy, feeding methane as “food” or “fuel,” may be placed between autotrophy and heterotrophy, because methane can be placed between inorganic and organic matter [85]. For most methanotrophs, methane serves as the dual sources for metabolic energy (catabolism, dissimilation) and biomass production (anabolism, assimilation). In this context, if methane is taken as half-organic and half-inorganic, methanotrophs are accordingly regarded as half-autotrophs and half-heterotrophs. However, the “type X” (or type Ib) methanotrophs and Verrucomicrobia-related methanotrophs are known to possess the CO2-fixing enzyme, RuBisCO, and assimilate CO2 via the Calvin-Benson cycle [86], and they are probably more widespread than previously presumed [87, 88].

Anaerobic oxidation of methane (AOM) is also a form of methanotrophy that is conducted by more than one microbial species, that is, archaeal-bacterial consortia, as described earlier. Both archaeal methanogens and bacterial sulfate-respirers (sulfate-reducing bacteria) are reported to assimilate CH4-derived (CH4-oxidized) CO2 autotrophically via the Calvin-Benson cycle [89].

4.2. Tubeworms

The gutless tubeworms, or siboglinid veriforms, represent the most enigmatic and intriguing organisms of the seep fauna in terms of body plan, morphology, life cycle, metabolisms, endosymbioses, and so on [90]. The first specimen of the gutless tubeworms was dredge-sampled in 1900 during the Siboga Expedition (1899–1900) from 462 m deep, off Selayar Island, Flores Sea, Indonesia [91], where methane seepage is presumed to occur in the active margin [92], and was later described as the new species S. weberi Caullery, 1944 [93], with proposals of the new genus Siboglinum Caullery, 1914, and the new family Siboglinidae [94] (Note 4).

Thereafter, siboglinid worms, typically >10-mm long and <1-mm wide, were collected sporadically from various oceanographic sites. Due to their unique and enigmatic body plan with no mouth, no anus, and no digestive tract, their way of living was interpreted to depend on dissolved organic matter absorbed from somewhere of body surface including the anterior “beard”; they were often called “beard worms.” The interpretation was based on the common belief that animals are heterotrophic. The heterotrophic animal view is still correct even now in a strict sense (that siboglinid worms depend eventually on organic matter produced by symbiotic bacteria), but the less-defined phrase “autotrophic animal” was advocated for siboglinid worms in a broad sense [66].

The gutless siboglinid worms often host a single thiotrophic endosymbiont species. A non-vent, non-seep gutless tubeworm (S. poseidoni Flügel and Langhof, 1983) harbors a methanotrophic symbiont [72, 73] probably of one species. However, gutless tubeworms may occasionally possess a single but probably methanotrophic endosymbiont, or thiotrophic but multiple endosymbionts. For example, the sediment-dwelling Oligobrachia mashikoi Imajima, 1973, hosts a symbiont that bears the genes of methanotroph-related 16S rRNA and CO2-fixing enzyme RuBisCO, suggesting the possible involvement of a CO2-fixing methanotroph, that is, “type X” or type Ib methanotroph [95]. Another sediment-dwelling worm (S. poseidoni) also has a methanotrophic endosymbiont [73]. Regarding multiple symbioses, some individuals of Lamellibrachia sp., currently described as Lamellibrachia sagami Kobayashi et al. [96], from the off-Hatsushima seep, Sagami Bay, central Japan, were reported to have four distinct thiotroph-like symbionts in their trophosome tissue [97, 98, 99, 100], and L. anaximandri Southward, Andersen and Hourdez, 2011, despite vent-dwelling, also hosts multiple thiotrophic species as endosymbionts [76].

Due to their unique and enigmatic body plan, their taxonomic position and status have been confused and subject to not a few, not minor changes ( Table 4 ), and still investigated by modern phylogenetic and phylogenomic approaches [101, 102]. As to their physiology, the “giant tubeworm” or R. pachyptila that inhabits hydrothermal vents is probably the most popular, well known, and well studied. The methane seep counterparts would be L. luymesi van der Land and Nørrevang [103] and Escarpia laminata Jones, 1985, inhabiting the base of Florida escarpment in the Gulf of Mexico [104], which are known to have extreme longevities as long as possibly >300 years [105, 106, 107].

Current236 accepted
32 accepted
2015Lamellibrachia sagami Kobayashi, Miura and Kojima, 2015 [96]
[94, 161, 162]
1985Escarpia spicata Jones, 1985,
Escarpia laminata Jones, 1985 [104]
1981Riftia pachyptila Jones, 1981
1975Lamellibrachia luymesi van der Land and Nørrevang, 1975 [103]
1964Lamellibrachia barhami Webb, 1969 [164]Lamellibrachia
1944Siboglinum weberi
Caullery, 1944 [93]

Table 4.

Taxonomic changes in positions and statuses of “gutless tubeworms” (mostly belonging to the class Polychaeta) that inhabit hydrothermal vents and methane seeps.

Other marine gutless worms (mostly belonging to the subclass Oligochaeta, class Clitellata) are not listed. Only accepted highest taxa, that is, accepted parents, as well as representative species and genera, are listed with accepted references. Current supra-taxa are also listed but in parentheses. Currently (as of May 2018), the family Siboglinidae is the highest taxon (parent) of all the vent/seep gutless tubeworms.

The giant tubeworm R. pachyptila grows quickly to >2 m high as far as the worm can uptake sulfide emitted from the vents ( Figure 4A ). By contrast, the seep tubeworm L. luymesi may also grow over 2 m long (not high) only slowly over >200-year longevity [108], as well as E. laminata may grow over 300 years [107]. Individual worms of the colonies of Lamellibrachia Webb 1969 often look “trimmed” within the limits of seeped methane/sulfide ( Figure 4B ). Not only trimmed, their bodies are often twisted to crawl on seafloor and even buried in the sediment. It has been pointed out that the posterior extension, or “root,” of Lamellibrachia worms functions to “sip” sulfide from the sulfate–methane transition zone (SMTZ) in the sediment [109] as well as to “dump” sulfate and protons (H+) to SMTZ [110]. Sulfate dumped into or below SMTZ will facilitate anaerobic oxidation of methane (AOM) with sulfate, and sulfide will be regenerated from the dumped sulfate and protons via AOM.

Figure 4.

The gutless tubeworms of a hydrothermal vent and a methane seep. (A) Riftia pachyptila Jones, 1981, inhabiting a vent site of the East Pacific rise at 2500 m depth [167]. (B) Lamellibrachia luymesi van der Land and Nørrevang [103], from a methane seep at 550 m depth in the Gulf of Mexico. The blue-stained tube indicates approximately 14 months of growth [168]. Photograph by Charles R. Fisher.

A whole process including symbiotic thiotrophy (aerobic oxidation of sulfide) and AOM in sediment may be viewed as an “extended symbiosis” that circulates the regeneration of sulfide and sulfate as if it functions as a “coffee percolator” (Note 5). The H2S/SO4 2− percolator is driven by methane supplies, eventually leading to the generation of CO2-HCO3 -CO3 2− from methane and thus to authigenesis of carbonates. The Lamellibrachia worms are often associated with carbonates and even incorporated in carbonates occasionally to form conglomerates as discussed later ( Figure 5 ).

Figure 5.

The seep tubeworm Lamellibrachia sagami Kobayashi et al. [96], being embedded in authigenic carbonate formed in the off-Hatsushima methane seep at 1100 m depth, Sagami Bay, Central Japan. The width of the photograph corresponds to 7 cm. Photograph by the author.

The tubeworm soft tissue that contains an amount of endosymbiotic thiotrophic bacteria is relatively higher (more enriched) in δ13C than soft tissues of mussels and clams of the same seep ( Figure 3 ) [46]. Tubes of the worms show intermediate δ13C values compared with those of soft tissues, with a weak tendency of δ13C becoming heavier toward the posterior end of the tubes [104]. This may be associated with the phenomenon that lower (more depleted) δ13C values are seen in the tubeworm-associated high-Mg carbonates than those colonized by Bathymodiolus mussels [39, 50, 57, 111].

4.3. Mussels

The mussels belonging to the genus Bathymodiolus Kenk and Wilson, 1985, represent the vent and seep fauna as well and harbor endosymbiotic bacteria eventually in their gills. While juveniles of vent mussels host epi-symbionts almost everywhere on their surfaces, endosymbiotic colonization becomes restricted to gill tissue during the mussel growth [112], and even adults are subject to continued bacterial colonization attacks throughout their lifetimes [113]. Although the process was observed with vent Bathymodiolus mussels, it may similarly occur to the seep Bathymodiolus mussels, as it is known for the shallow-water tropical lucinid clam Ctena orbiculata (Montagu, 1808) cited as its synonym Codakia orbiculata (Montagu, 1808) [114].

Their endosymbionts are thiotrophs or methanotrophs or both. The vent mussel B. thermophilus Kenk and Wilson, 1985, in the East Pacific Rise has only thiotrophic symbionts [66, 115], while the seep mussel B. childressii Gustafson, Turner Lutz and Vrijenhoek, 1998, in the Gulf of Mexico hosts only methanotrophic symbionts [70]. A vent Bathymodiolus species in a western Pacific harbors a CO2-fixing methanotroph, that is, “type X” or type Ib methanotroph [116].

Dual symbiosis, in which a single host harbors both thiotrophic and methanotrophic bacteria, has been described for seep mussels from the Gulf of Mexico (B. brooksii Gustafson, Turner, Lutz and Vrijenhoek, 1998) [71], off Congo passive margins [78] and other seep mussels, as well as vent mussels. A vent Bathymodiolus mussel is known to harbor hydrogen-oxidizing autotrophic bacteria [79], which process is now regarded as probably more widely and ubiquitously distributed in deep-sea environments [83].

The small mytilid mussel, Idas sp., inhabiting carbonate crusts at the off-Nile fan seep harbors six endosymbionts probably of thiotrophs, methanotrophs, and previously unrecognized roles [117]. Similarly, B. heckerae Turner, Gustafson, Lutz and Vrijenhoek, 1998, inhabiting the “asphalt” seep in the Gulf of Mexico [118, 119] harbors multiple endosymbiotic bacterial species, one of which belongs probably to the genus Cycloclasticus Dyksterhouse, Gray, Herwig, Lara and Staley, 1995 [120]. The symbiotic Cycloclasticus appeared to degrade and derive carbon and energy from short-chain alkanes such as ethane and butane [121], despite lack of genes responsible for the degradation of polyaromatic hydrocarbons that are seen in other Cycloclasticus species [122].

Overall, it can be said that the seep mussels possess high plasticity and flexibility in harboring and depending on a variety of endosymbionts and their energetic metabolisms: from single via dual to multiple symbioses with thiotrophs and methanotrophs via hydrogenotrophs to asphalt-degrading heterotrophs. This symbiotic plasticity may facilitate evolution and ubiquity of these mussel species [123, 124, 125].

The Bathymodiolus, as well as Idas, mussels attach and settle on hard substrates such as basalts in hydrothermal vents and carbonates in methane seeps, like tubeworms do. However, Bathymodiolus mussels tend to colonize 13C-enriched carbonates, compared with tubeworm association with 13C-depleted high-Mg carbonates [39, 50, 57, 111].

4.4. Clams

The “giant white clams” or the vesicomyid clams belonging to the genes Calyptogena Dall, 1891, also represent the fauna of both hydrothermal vents and methane seeps. They are mostly dependent on endosymbiotic bacterial thiotrophs for their nutrition, not on methanotrophs [74]. However, a thyasirid clam, Axinulus hadalis Okutani et al. [126], living within (but a few meters deeper from) the deepest methane seep community [127], was reported to have dual endosymbionts, which were speculated to be thio- and hydrogenotrophs, that is, sulfur- and hydrogen-oxidizing chemoautotrophs, respectively [128].

The Calyptogena clams are semi-endobenthic and live half-buried in the sediment between and around carbonate rocks. Therefore, the clams are not associated with carbonate rocks for living, although they occur in close vicinities. This may be confirmed by the difference in δ13C values of the clam shells and carbonate rocks, which would reflect different carbon sources despite their habitat vicinities [129].

5. Conglomerates of carbonates and tubeworms

Authigenic carbonates “grow” in the zone anaerobic oxidation of methane (AOM) and sulfate–methane transition zone (SMTZ) in the sediment of methane seeps, as shown by low δ13C values. Similarly, the gutless tubeworms such as Lamellibrachia species grow toward posterior rather than anterior to “percolate” (exploit and regenerate) sulfide in the horizon of AOM zone overlapped with SMTZ, also as indicated by the tendency of lower δ13C toward the posterior end of the tube [24]. Sipping of sulfide and dumping of sulfate at the root (posterior end) of the tubeworms may change the local pH and thus affect the conditions for favored formation calcite to aragonite [57, 130]. These growths of authigenic carbonates and autotrophic tubeworms occur concomitantly near the posterior of worm tubes [130] and often intercalate each other to form mineral-animal “conglomerates” ( Figure 5 ). Although detailed observation suggested that a nodular high-Mg calcite is formed before tubeworm settlement [130], the coupling of high-Mg calcite and tubeworm colonization has not been elucidated.

The conglomerates of calcite and L. sagami in the off-Hatsushima methane seep, Sagami Bay, central Japan, were studied with reference to δ13C and Mg contents and were compared with those from the past authigenic carbonate formed in the Miocene, 17.2–14.4 million years ago (Ma), from the Hayama Group, Miura Peninsula, central Japan. The two sites, that is, modern and past methane seeps, are only <50.0 km distant, and the data from the modern and past carbonates revealed that the high content (~15.0%) presence of Mg in relatively high δ13C (<30.0‰ against >30.0‰) calcite is closely associated with conglomeration with tubeworms in both modern and fossil specimens ( Table 5 ) [3, 100, 131].

Modern carbonate in the off-Hatsushima methane seep, Sagami BayMiocene carbonate (17.2–14.4 Ma), Hayama Group, Miura Peninsula
With tubewormsWithout tubewormsWith fossil tubesWithout fossil tubes
δ13C−28.0 to −27.0‰−34.0 to −33.0‰Not determined
CaCO3 (%)34.0–43.052.0–86.039.0–40.066.0–67.0
MgCO3 (%)12.0–15.0<0.1014.0–15.0<0.10
FeO2 (%)4.00–6.005.00–15.04.00–5.0028.0–29.0
SiO2 (%)28.0–31.0<0.10–37.028.0–29.0<0.10
AlO2 (%)9.00–10.0<0.10–12.09.00–10.0<0.10

Table 5.

Comparison of δ13C values (‰) and compositions of selected chemical species (weight-to-weight %) in modern and Miocene carbonates with reference to the presence/absence of living tubeworms or fossil worm tubes [3, 100, 165, 166].

6. Conclusive remarks

Authigenic carbonates and autotrophic faunas provide unique and typical landscapes of methane seeps ( Figures 1 and 2 ). The carbonates and faunas are formed and maintained not independently but interactively via microbial activities of methanogenesis, anaerobic (and aerobic) oxidation of methane, anaerobic respirations such as sulfate reduction, and carbonate (particularly dolomite) formation. During these microbial processes, the stable carbon isotope ratios (δ13C values) do shift with respective ranges of isotopic fractionation (Δ13C, Tables 2 and 3 ). Not only microorganisms but also macro-fauna may contribute to form and shape authigenic carbonate rocks. In the case of rock-tubeworm conglomerates, tubeworms actively recycle sulfide and sulfate in sediment, resulting in the acceleration of “growth” of the conglomerates.


The author is obliged to the crew and operation teams of manned and unmanned deep-sea vehicles and support ships of the Japan Agency for Marine-Earth Science and Technology (JAMSTEC) for deep-sea expeditions. The photograph of the methane seep landscape ( Figure 1 ) was courteously provided by JAMSTEC.

Conflict of interest

The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.


(Note 1) In the strict sense, chemolithoautotrophy should be used instead of lithotrophy or chemoautotrophy; however, the term is only used by experts in rather a narrow area of microbiology and sounds too technical for non-expert audience.

(Note 2) Endosymbiosis is widespread in non-vent, non-seep organisms [123]. Chemoautotrophic bacterial endosymbiosis was characterized with the gutless oligochaetes Inanidrilus leukodermatus (Giere, 1979) from 5-m-deep sediment in a Bermuda inlet [135] and Olavius crassitunicatus Finogenova, 1986, from 270- to 359-mdeep sediment in the Peruvian passive margin [136], as well as a marine nematode Astomonema sp. from coral reef sediments in the Bahamas [137]. Multiple endosymbiosis of the gutless oligochaete Olavius algarvensis Giere, Erséus and Stuhlmacher, 1998, was subject to genetically and biochemically dissected by metaproteomics [138] that revealed unusual pathways, for example, use CO and H2 for energetic metabolism [139]. Animal-bacterial chemo−/methanotrophic symbioses have recently been recognized as more widespread and ubiquitous in anaerobic sediments, besides vents, seeps, and organic falls, than previously presumed [140]. A microbiome of an individual of the gutless oligochaete I. exumae Erséus, 2003, differs markedly from those of other 22 individuals [141], which also demonstrates the symbiotic plasticity that may facilitate the adaption and evolution of this group of the gutless tubeworms.

(Note 3) Anaerobic oxidation of sulfide with nitrate, which is anaerobic thiotrophy (thioautotrophy) based on nitrate-respiration, is seen in bacterial species belonging to the genus Beggiatoa Trevisan, 1842 [132]. This energetic metabolism was once expected for the endosymbiont of the hydrothermal vent tubeworm (R. pachyptila Jones, 1981) [133], but the possibility was denied later [134].

(Note 4) Maurice Jules Gaston Corneille Caullery (1868–1958), a French zoologist, studied the first specimen of the “beard worm” and proposed the new family Siboglinidae and new genus Siboglinum Caullery, 1914, presumably named after the Dutch “Siboga” Expedition (1899–1900), during which the specimen was dredge-sampled. “Siboga” was the name of the vessel, which originally was a 50-m-long gunboat owned by the government of the Dutch East Indies [142]. Caullery described the new family Siboglinidae in 1914 based on the simultaneously proposed new genus Siboglinum. The type species of the genus, S. weberi Caullery 1944, was described subsequently 30 years later, in 1944. It is reasonably considered that the specific epithet “weberi” was named after the leader of the “Siboga” expedition, Max Carl Wilhelm Weber, a German-Dutch zoologist.

(Note 5) The sulfide/sulfate “percolator” in the seep system can be viewed as “extended symbiosis” between gutless host tubeworms, thiotrophic endosymbionts, and sulfate-consuming AOM microbial consortia. In these relationships, biologically true symbiosis is postulated only between host worms and internal thiotrophs, and the involvement of external AOM consortia is regarded as “extended”. By contrast, true endosymbiosis of a host worm and two bacterial symbionts, that is, dual symbiosis of sulfur-oxidizing and sulfate-reducing bacteria is seen in the gutless oligochaete worm Olavius algarvensis Giere, Erséus and Stuhlmacher, 1998, and Olavius crassitunicatus Finogenova, 1986, that host multiple (more than dual) endosymbionts [136, 143].

© 2018 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution 3.0 License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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Takeshi Naganuma (August 1st 2018). Geo-Biological Coupling of Authigenic Carbonate Formation and Autotrophic Faunal Colonization at Deep-Sea Methane Seeps II. Geo-Biological Landscapes, Marine Ecology - Biotic and Abiotic Interactions, Muhammet Türkoğlu, Umur Önal and Ali Ismen, IntechOpen, DOI: 10.5772/intechopen.78978. Available from:

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