5.1 Background

5.1.1 Cold Seeps in the South China Sea

Since the first report of hydrocarbon seeps in the South China Sea (SCS) in 2005, more than 40 seep sites have been discovered, mostly distributed in the northern SCS (Suess et al. 2005; Chen et al. 2006; Niu and Feng 2017; Wang et al. 2022). Among them are three active seep areas—two located off southwest Taiwan (Yam seep and Site F), and the other off Hainan (Haima cold seep) (Fig. 5.1). The Yam seep (Tseng et al. 2023), located on the Four Way Closure Ridge with a depth around 1500–1700 m, is characterized by low seepage intensity. Little is known about the epifaunal community of the Yam seep, except for the presence of the bathymodiolines Gigantidas platifrons and Bathymodiolus securiformis (Klaucke et al. 2016; Kuo et al. 2019). Site F, located at the summit of Formosa Ridge—a small area of about 180 m × 180 m with well-developed authigenic carbonates at water depths around 1120 to1150 m, has been extensively surveyed in recent years (Lin et al. 2007; Feng and Chen 2015). The Haima cold seep is the largest active seep region in SCS, covering an area of around 350 km2 at water depths between 1350 to 1525 m. It is located in the Qiongdongnan Basin at the northwest continental margin of the SCS. Several epifaunal surveys have been conducted at Site F and Haima during the past decade, which have shed light on their epifaunal compositions and potential trophic relationships (Feng et al. 2015, 2018a; Zhao et al. 2020; Ke et al. 2022).

Fig. 5.1
A map of South China Sea for the distribution of active deep-sea hydrocarbon seep fields. They are located at Haima, Site F, and Yam.

Distribution of active deep-sea hydrocarbon seep fields in the South China Sea

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5.1.2 Seep Macrofauna of the South China Sea

Suess et al. (2005) was the first to systematically survey the SCS cold seeps in 2004, but in this cruise only inactive cold seeps were found in the northeastern slopes. He reported evidence of past seep activities, as shown by the extensive development of authigenic carbonate rocks at depths from 500–800 m. He also reported empty shells of bivalves that are supposed to host endosymbiotic chemosynthetic bacteria, including shells from a mud bottom with high concentrations of methane at 3000 m depth in Haiyang 4 area that were later identified as Archivessica nanshaensis (Li et al. 2023), and some vesicomyid clam and shells, and coral skeletons on authigenic carbonate rocks at the Jiulong methane reef.

Since the first discovery of an active cold seep in the SCS in 2007 (Lin et al. 2007; Machiyama et al. 2007), several studies of the cold seep epifauna have been conducted in this region, including Mollusca (Chen et al. 2018; Xu et al. 2019; Lin et al. 2022a), Annelida (Zhang et al. 2018; Xu et al. 2022), Crustaceans (Dong and Li 2015; Li 2015), Echinodermata (Li et al. 2021; Nethupul et al. 2022) and other taxa (Gong et al. 2015). Six studies have attempted to describe the epifaunal communities inhabiting the Site F and Haima cold seep (Feng et al. 2018a; Zhao et al. 2020; Xu et al. 2020; Dong et al. 2021; Ke et al. 2022; Wang et al. 2022). Feng et al. (2018a) presented a list of 30 species from six phyla, including eight species of Mollusca, 12 species of Arthropoda, three species of Annelida, two species of Porifera, one species of Cnidaria and four species of Chordata. They found only three common species (Gigantidas platifrons, Bathyacmaea lactea and Munidopsis verrilli) in two seep areas. Zhao et al. (2020) expanded the list of epibenthic animals at Site F to 28 species, including 10 new records. In the Haima region, Xu et al. (2020) reported six seep sites with various methane seepage strengths, and different macrofaunal communities, including HM-1 with clusters of Archivesica marissinica and empty Archivesica shells along with mussels and holothuroids, HM-2 with a dense G. haimaensis mussel bed and scattered Paraescarpia tubeworms at the edge, HM-3 with massive mussel beds and Phymorhynchus buccinoides snails, HM-4 with authigenic carbonates with empty Archivesica shells and a few holothuroids, HM-5 with carbonate mounds as a deep-sea fish habitat, and HM-6 with several patches of mussels. They reported species from 11 families and seven classes observed by video or photographic records. Dong et al. (2021) reported a total of 34 species, including 12 species of Mollusca, seven species of Arthropoda, two Annelida and one species of Echinodermata. More recently, Ke et al. (2022) reported a total of 30 species, including 13 species of Mollusca, six species of Arthropoda, seven species of Annelida and three other taxa. Among these, six were new records from the Haima area.

Besides reporting the biodiversity of cold-seep macrofauna, several studies have determined their stable isotopes (i.e., δ13C, δ15N, δ34S) (Feng et al. 2018b; Lin et al. 2020; Zhao et al. 2020; Ke et al. 2022; Wang et al. 2022), which contributed our understanding of the trophic modes of seep specialists and habitat generalists. For instance, Zhao et al. (2020), using a two-source stable isotope mixing model, estimated that methane contributed from 30% in the king crab Lithodes longispina to 91% in the mussel Gigantidas platifrons to the carbon pool of the common animals at Site F. Lin et al. (2020) constructed trophic models on seep and non-seep fauna off Taiwan. They found that the seep megafauna had specialized diet niches, whilst the seep-associated L. longispina was the top predator. Moreover, they also indicated that this king crab utilized energy from the neighboring deep-sea ecosystems.

Studies have also been conducted to unveil the genetic divergence and connectivity of seep macrofauna within the SCS (Yao et al. 2022), and between the SCS and nearby vent and seep ecosystems in Northwest Pacific (Shen et al. 2016; Yang et al. 2016; Xu et al. 2017, 2018, 2019, 2021; Xiao et al. 2020). These species have different life-history characteristics that may determine their dispersal routes (i.e., via bottom, mid-water or surface currents), dispersal distances, and genetic differentiation.

Evolutionary studies have also been conducted to reveal the genetic adaptations in cold seep macrofauna, including the evolution of the mitochondrial gene orders of deep-sea polynoids (Zhang et al. 2018) and bathymodiolines (Liu et al. 2018; Zhang et al. 2022), as well as the genome- or transcriptome-level metabolic complementarity between bathymodiolines (Sun et al. 2017; Lin et al. 2022b), vesicomyid clams (Lan et al. 2019; Ip et al. 2021), siboglinid tubeworms (Yang et al. 2019; Sun et al. 2021) and their symbiotic bacteria.

In this chapter, we summarize the previous research findings of seep macrofauna in the SCS and our new findings from cruises taken in 2021 and 2022. We focus on species diversity at the Haima and Site F seeps, and compare them with those vent fields and seep areas in the Northwest Pacific.

5.2 Faunal Species Diversity

We compiled a total of 81 seep-associated macrofauna from SCS, including 13 species that have not been reported in previous studies (Table 5.1). These species belong to eight phyla, 14 classes, and 34 orders, where 42 macrobenthos were identified to species level, 31 species were identified only to the genus level and the rest were assigned to high taxonomic ranks. They include 35 species reported from Site F and 58 species from Haima, and 10 species from both cold seep areas, including four molluscs (G. platifrons, “B.” aduloides, Phymorhynchus buccinoides, Bathyacmaea lactea), two polychaetes (P. echinospica and Branchipolynoe pettiboneae), three decapods (A. longirostris, M. lauensis and M. verrilli and one ophiuroid (H. haimaensis). Previous studies have pointed out the substantial differences in seep macrofaunal abundance and species compositions between Site F and Haima (Zhao et al. 2020; Dong et al. 2021; Ke et al. 2022). For instance, the mussel G. haimaensis and the limpet Bathyacmaea lactea were dominant at Haima, while the mussel G. platifrons and the limpet Bathyacmaea nipponica were dominant at Site F. The crustacean S. crosnieri at Site F, but it was not found at Haima. The sea anemone Actinernus sp., the tubeworm Sclerolinum annulatum and the clam A. marissinica were endemic to Haima cold seep. These observations imply that geographic settings along with other unknown abiotic and biotic factors may influence the spatial distribution and associated macrobenthic communities in these two seep areas.

Table 5.1 Species list of seep fauna in the South China Sea
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Site F and Haima host a total of 30, 21 and 11 species of molluscs, crustaceans and annelids, respectively. A previous study summarizing 42 vent and seep areas in the Northwest Pacific revealed 2 − 38 species of molluscs, crustaceans and annelids (Nakajima et al. 2014), therefore, the faunal diversity of the two seep areas in the SCS is relatively high.

5.2.1 Mollusca

Mollusca is the most diverse phylum of seep macrofauna in the SCS, with 30 species belonging to four classes, including 10 species of Bivalvia, 16 species of Gastropoda, three species of Polyplacophora, and one species of Cephalopoda. A total of eight species of molluscans have been recorded from Site F, and 25 from Haima. Among them, only G. platifrons, “B.” aduloides, Phymorhynchus buccinoides and Bathyacmaea lactea have been recorded from both cold seep areas. The bathymodioline mussels G. haimaensis, and Nypamodiolus samadiae, and the vesicomyid clam A. marissinica appear to be endemic to the SCS (Fig. 5.2a, b; Chen et al. 2018; Xu et al. 2019; Lin et al. 2022a).

Fig. 5.2
A set of underwater pictures, a to m. A has a mussel bed. B is a zoom-in of a clam bed. C has a sheet-like layer of siboglinid tubeworms. D has empty clam shells on the seabed. E has a zoomed-in mussel bed. F has a shrimp stuck to the apparatus over shrimp bed. G has a zoomed-in photo of Alvinocaris longirostris on the mussel bed. H has a hermit crab on sand. I to m are photos of different deep-sea species with mussel beds.

Common seep macrofauna in the Haima cold seep region. a mussel bed (dominated by Gigantidas haimaensis); b clam bed (Archivesica marissinica); c siboglinid tubeworms (Sclerolinum annulatum; Xu et al. 2022); d glass scallops (Catillopecten sp.) on empty clam shells; (e) epibenthos on mussel beds, including Actinernus sp., Puncturella sp., Provanna spp., Munidopsis lauensis, Histampica haimaensis; f swimming shrimp around mussel beds (Nematocarcinus sp.); g Alvinocaris longirostris on the mussel bed; h two hermit crabs on mud surface near a clam bed and one carried an orange sea anemone (Hormathiidae gen. et sp.); i–m some swimming deep-sea species, including Chordata, jellyfish and sea cucumber (Paelopatides sp.). Water depth of above species, ~1360–1430 m. Photographed by ROV “Pioneer”

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Most non-symbiotic molluscan species live on mussel beds. At Site F, six of the reported molluscs are non-symbiotic, i.e., Enigmaticolus nipponensis (previously named as E. inflatus, see Chen et al. 2020b), Provanna snails and Bathyacmaea limpets were commonly found on mussel beds of G. platifrons. The octopus Benthocopus sp. might not be a seep-endemic species; it might take advantage of the large amount of bathymodiolines as potential food resources, but this hypothesis needs to be tested with further stable isotope and gut content analyses. Likewise, most non-symbiotic molluscs at Haima are mainly observed on the G. haimaensis mussel beds (Fig. 5.2e). A specimen of the grey limpet Puncturella sp. was collected during a 2022 cruise, but it is not as common as Bathyacmaea lactea. The large gastropod P. buccinoides sometimes form as dense aggregates on the edge of mussel beds and clam beds, which often move along the same direction. Yoldiella sp., a small bivalve (often less than 1 cm) previously identified as Malletia, was commonly found in sediment of the mussel beds, clam beds and tubeworm clusters. The glass scallops Catillopecten sp., previously identified as Propeamussium sp. (Dong et al. 2021; Ke et al. 2022), formed a small aggregate on the empty clam shells (Fig. 5.2d), and have been found swimming into the water column when disturbed.

At Site F, G. platifrons is the dominant species, which harbors symbiotic methane-oxidizing bacteria (MOB; Gammaproteobacteria) inside its gill epithelial cells (Sun et al. 2017), and sulfur-oxidizing bacteria (SOB; Campylobacteria) on the gill surface (Sun et al. 2022; Lin et al. 2022b). “Bythymodiolus” aduloides, which is rare at both Site F and Haima, also harbors symbiotic SOB in its gill epithelial cells (Lorion et al. 2009). While, at Haima, seven reported bivalves, i.e., four from Bathymodiolinae, one from Solemyidae, one from Lucinidae and one from Pliocardiinae, are known for their association with symbiotic chemosynthetic bacteria (Sun et al. 2017; Ip et al. 2021). Gigantidas haimaensis dominates the seepage area, forming mussel beds and providing shelters for many other macrobenthos (Fig. 5.2a; Xu et al. 2019). The other three bathymodiolines are rare: a few G. platifrons and N. samadiae were observed within mussel beds of G. haimaensis while “B.” aduloides individuals were found on carbonate rocks surrounding a P. echinospica cluster. The different community structures, habitat preferences and abundances reflect the availability of methane and hydrogen sulfide in their habitats. These characteristics are reflected in their stable isotope compositions. The δ13C values of G. platifrons (–66‰ in Site F) and G. haimaensis (~–50‰ in Haima) are low, indicating methanotrophic nutrition, whereas the other two bathymodiolines have δ13C values of ~–35‰, inferring their thiotrophic nutrition (Feng et al. 2018b; Ke et al. 2022). In fact, G. platifrons and G. haimaensis harbor not only endosymbiotic gammaproteobacterial MOB, but also epibiotic campylobacterial SOB on gill surface, although the function of the epibionts remains unclear (Lin et al. 2022b). In addition, “B.” aduloides and N. samadiae symbiosis with gammaproteobacterial SOB in their gill cells, and these symbionts are closely related to those of other bathymodioline endosymbionts (Lorion et al. 2009; Lin et al. 2022a). Moreover, the gill epithelial cells of N. samadiae also harbor Spirochaetes, but their function in the host’s nutrition and other aspects of biology such as immunity is unknown (Lin et al. 2022a). While the bathymodiolines are found on the surfaces of sediment or authigenic carbonate rocks, the other three bivalves are semi-infaunal or infaunal. The vesicomyid clam Archivesica marissinica lives at the edge of mussel assemblages or away from mussels with half of their shells buried into the sediment (Fig. 5.2b). Like other vesicomyids, they extend their foot into the sediment to obtain hydrogen sulfide from the pore water and extend their inhalant siphon into the water column to pump in oxygen- and carbon dioxide-rich water. Its gill epithelial cells harbor chemosynthetic SOB (Lan et al. 2019; Ip et al. 2021), as indicated by δ13C value of ~ –35‰ (Ke et al. 2022). Different from the bathymodiolines that are inferred to obtain their symbionts from the ambient environment via horizontal transmission during the larval development in each generation, these vesicomyids transfer their symbionts from parent to offspring via maternal transmission (Funkhouser and Bordenstein 2013). As long-term obligate intracellular lifestyle has promoted genetic drift, the endosymbionts’ genome size has been greatly reduced, missing many genes required for free living, including cellular envelope, signal transport, environmental sensing, motility, cell cycle control, and recombination (Ip et al. 2021). Acharax sp. (identified as Solemya sp. in Dong et al. 2021) and Thyasira sp., also bearing chemosynthetic symbionts (Giudice and Rizzo 2022; Taylor et al. 2022), were discovered from sediment samples collected in the margins of mussel beds and clam beds. Both species are rare at Haima, and their detailed symbiotic relationships have not been analyzed, although they are expected to be associated with SOB.

5.2.2 Arthropoda

Arthropoda is the second largest phylum among the reported seep macrobenthos, consisting of 21 seep specialists and non-seep obligate species, among them Uroptychus jiaolongae and U. spinulosus have been reported only from Site F. Among the 21 species, 12 were from Haima and Site F, respectively, and two of them were found in both seep areas. Shinkaia crosnieri, although very abundant at Site F (Zhao et al. 2020), is absent at Haima. Alvinocaris and Munidopsis are common on mussel beds of both seep areas (Fig. 5.2e, g). Alvinocaris shrimps are frequently sheltered among mussels while Munidopsis sp. are distributed on mussels. Three species of Munidopsis have been reported from the SCS seeps, but it is impossible to distinguish them from videos or photographs taken on-site. Alvinocaris longirostris is commonly found on mussel beds. Having been reported from vents in the Manus Basin (Wang and Sha 2017) and Okinawa Trough (Watanabe and Kojima 2015), and a seep in Sagami Bay (Fujikura et al. 1996), A. longirostris is perhaps the most widely distributed species among the animals inhabiting chemosynthetic ecosystems in western Pacific. Alvinocaris kexueae, reported herein for the first time from the SCS seeps, has been reported from the Manus Basin only (Wang and Sha 2017). These shrimps rely on a consortium of chemosynthetic bacteria comprising mainly SOB on their gill surface for nutrition, which is reflected by their stable isotope signature (δ13C value: ~ –42‰ to –40‰; Ke et al. 2022). Shinkaia crosnieri obtains nutrition by feeding directly on episymbiotic bacteria grown on the chaetae that are densely distributed on their ventral side (Watsuji et al. 2014), but its dietary composition may shift during ontogenetic development from a dominance of SOB to a dominance of MOB, indicated by ~ –54‰ to –42‰ δ13C value for individuals of different sizes (Zhao et al. 2020).

At Haima, opportunistic scavenging amphipods Eurythenes maldoror and Parallcella sp. and the isopod Bathynomus jamesi have been captured using trap nets. Large crabs Neolithodes brodiei and Paralomis sp. have been captured using either scoop nets or directly using the manipulators of the ROV. Although no stable isotope data are available for some crabs, they should be opportunistic predators not specific to seepages like Chaceon manningi, Lithodes longispina and Glyphocrangon sp. found at Site F (Zhao et al. 2020; Ke et al. 2022). We also collected two hermit crabs from Haima in 2022 (Fig. 5.2h), one in the family Parapaguridae associated with a sea anemone. Currently, no detailed taxonomic information is available for these hermit crabs.

5.2.3 Annelida

A total of 11 species of annelids are known in the SCS seeps, including two species of Sabellida, six species of Phyllodocida, one species of Terebellida and two species of Scolecida. Among them, eight species have been recorded from Haima and five from Site F, with only two of them recorded from both cold seep areas (Table 5.1).

As important modifiers of local habitats, Siboglinid tubeworms are among the conspicuous fauna in cold seeps. Both siboglinid tubeworms (Sclerolinum annulatum and Paraescarpia echinospica) in the SCS form dense tube bushes, with their roots extending deep into the sediment. Paraescarpia echinospica forms dense populations at Haima, but it is rare at Site F (Zhao et al. 2020). While Sclerolinum annulatum (Fig. 5.2c) forms dense patches at Haima only (Xu et al. 2022). Both tubeworm species harbor thiotrophic gammaproteobacterial SOB as the electron donor for energy production and nutrition (Yang et al. 2019; Sun et al. 2021; Xu et al. 2022).

Three species of scale worms, including Branchipolynoe pettiboneae, Branchinotogluma cf. japonicus, and Lepidonotopodium cf. okinawae, have been reported from Site F, while only B. pettiboneae has been recorded from Haima. Branchipolynoe pettiboneae is a parasite of the bathymodiolines G. haimaensis and G. platifrons in the SCS, commonly found in their mantle cavity. The other two species are free-living, having been found crawling on bathymodioline shells or authigenic carbonate rocks.

Amphisamytha sp., a deposit feeder living inside their self-secreted membrane tubes, has been found only at Site F, with their tubes attached to the carapace and claws of S. crosnieri. Two infaunal species (Capitella sp. and Nemache sp.) and three free-living species (Glycera sp., Nereis sp. and Sisoe sp.) have been recorded at Haima seep, although these species have yet to be identified at species level.

5.2.4 Other Taxa

Seven species of Echinodermata have been recorded from the SCS seeps. Among them, the holothuroid Chiridota heheva and the ophiuroid Histamipica haimaensis are abundant at Haima. Histampica haimaensis in the SCS has not been reported from elsewhere, but C. heheva is widely distributed from seeps, vents and wood-falls in Gulf of Guinea, Southwest Indian Ridge and Cayman Rise (Thomas et al. 2020). Histampica haimaensis is common on bathymodioline shells, and P. echinospica and S. annulatum tubes. C. heheva often lies on mussel beds and clam beds, as well as bare sediment surfaces. In addition to H. haimaensis, two other morphologically distinct ophiuroids have been discovered in this region. Ophiophthalmus serratus (Nethupul et al. 2022) is big, with a disc length of ~ 15 mm and the disc having granules on the dorsal side and no plates and exposed radial shield. It has a similar distribution to H. haimaensis, but its abundance is much lower. Amphiuridae sp., with a disc length of ~ 10 mm, is rare in this region. It is easily distinguished from the other two species by having a basal-linked radial shield.

In 2022, we found two individuals of brown-color sediment-burying echinoids at Haima belonging to the suborder Paleopneustina. This is the first echinoid species discovered in SCS seeps, but its species identity remains unknown. A purple-color holothuroid (Paelopatides sp.) was found swimming around the seep site. Members of this genus of sea cucumbers are common in the Pacific Ocean (Fig. 4. in Martinez et al. 2019). At Site F, the starfish Pteraster sp. (Zhao et al. 2020) and the brittle star H. haimaensis (Li et al. 2021) are the only reported echinoderms. Like many annelids, most seep echinoderms in the SCS have not been identified at the species level.

Several species of minor taxa, including Platyhelminthes, Porifera and Cnidaria have also been reported from the SCS seeps. A species of Platyhelminthes (Discocelidae gen. et sp.) was first found on mussel beds of the Haima in 2022, but its species identity is unknown. Two species of Porifera (Semperella jiaolongae and Euplectellidae gen. et sp.) and two species of soft corals (Anthomastus sp. and Chrysogorgia sp.) were reported from Site F (Gong et al. 2015; Li 2017; Zhao et al. 2020). Two species of sea anemones were found only at Haima, including the purple Actinernus sp., which commonly attached to shells or on the sediment surface, and the orange Hormathiidae gen. et sp., which was rare, with only a few individuals observed on the sediment surface close to mussel beds or clam beds, as well as on the shell of a hermit crab (Fig. 5.2h).

Several species were captured at the seep areas by videos during previous research cruises but were not captured physically, such as an unidentified jellyfish, a swimming holothuroid (Paelopatides sp.) and fishes (Fig. 5.2i–m). The raindrop fish Psychrolutes inermis has been found in both seep areas, often staying on mussel beds (Xu et al. 2020; Zhao et al. 2020). Given its low mobility and its eggs were found on carbonate rocks (Xu et al. 2020; but it was mistakenly identified as Spectrunculus grandis), this fish species is likely a seep specialist, potentially depending on other seep animals for nutrition. Species of Coryphaenoides, Synaphobranchus, Bathypterois and Hydrolagus fishes were commonly found swimming the above seep areas. Given their strong mobility, they are like opportunity predators seeking food in the seep areas but not specific to these chemosynthetic habitats.

5.3 Connectivity with Other Northwestern Chemosynthetic Ecosystems

Quite a few chemosymbiotic species and non-chemosymbiotic taxa discovered in the SCS seep communities have also been reported from other vent and seep fields in the Northwest Pacific (Watanabe et al. 2010; Xu et al. 2020; Zhao et al. 2020; Dong et al. 2021). Dong et al. (2021) suggested that the community structure of Haima cold seep is similar to that of chemosynthesis-based communities in Sagami Bay (Fujikura et al. 2012). That needs more evidence, considering Paraescarpia echinospica also distributed in Site F and some vents and some species are endemic to Haima (G. haimaensis, A. marissinica, N. samadiae etc.). In contrast, the seep community at Site F is similar to that of the hydrothermal vents in the Okinawa Trough owing to the “G. platifrons– S. crosnieri” assemblage and other non-symbiont species (Watanabe and Kojima 2015; Feng et al. 2018a; Zhang et al. 2018; Dong et al. 2021). They share several symbiont-hosting species (i.e., G. platifrons, “B.” aduloides, S. crosnieri, A. longirostris and P. echinospica), and quite a few non-symbiont hosting taxa. This high faunal similarity in the two regions indicates that the seep and vent animals may share some common environmental requirements, although that are supposed to be quite different (Levin et al. 2016).

Recent rapid advances in molecular technologies have enabled us to decipher the connectivity and biogeography of deep-sea organisms from a genomic perspective. To date, population genomic studies based upon genome- or transcriptome-wide single-nucleotide polymorphisms (SNPs) have been performed on three dominant macrofauna species in the Northwest Pacific, including the bathymodioline mussel G. platifrons (Xu et al. 2018), the munidopsid squat lobster S. crosnieri (Chen et al. 2020a; Xiao et al. 2020), and the patellogastropod limpet B. nipponica (Xu et al. 2021). Among them, G. platifrons and B. nipponica both spawn eggs into the water column for fertilization, with larvae of G. platifrons possibly being planktotrophic while those of B. nipponica being lecithotrophic (Chen et al. 2019; Ponder et al. 2020). By contrast, females of S. crosnieri brood oil-rich eggs attached to the pleopod and were inferred to produce lecithotrophic larvae (Miyake et al. 2010).

With the application of genome-wide SNP markers, two semi-isolated lineages of G. platifrons were discovered in the Northwest Pacific (Xu et al. 2018). One was in the seep area at Site F and the other spanned vent fields in the Okinawa Trough and the Off Hatsushima seep in Sagami Bay (Xu et al. 2018). Additionally, a minor genetic divergence was revealed between its local populations in the the southern Okinawa Trough and those across the middle Okinawa Trough and the Sagami Bay (Xu et al. 2018). Similarly, with the application of either genome-wide SNPs or transcriptome-wide SNP markers, two genetic groups of S. crosnieri have been detected in the Northwest Pacific, including one at Site F and the other at the vent fields in the Okinawa Trough (Chen et al. 2020b; Xiao et al. 2020). In comparison, four habitat-linked genetic groups were characterized for B. nipponica in the Northwest Pacific by using genome-wide SNP markers (Xu et al. 2021). Among them, three seep genetic groups distributed at Site F in the SCS, the Kuroshima Knoll seep in the Ryukyu Arc, and the Off Hatsushima seep in Sagami Bay, respectively, while one vent genetic group dwelled in hydrothermal vents across the southern to middle Okinawa Trough (Xu et al. 2021).

The genetic differentiation patterns of the three deep-sea macrofaunal species collectively highlight the barrier effect of the Luzon Strait: potentially due to the relatively small amount of water involved, the Luzon Strait may represent a genetic barrier or serve as a dispersal barrier to facilitate the genetic divergence of deep-sea species that inhabit its two sides (Xu et al. 2018, 2021). Furthermore, the discordances in genetic divergence of these three deep-sea macrofauna imply the differences in life-history traits and/or environmental adaptabilities or habitat types may have played vital roles in shaping their population connectivity and biogeographic patterns (e.g., Xiao et al. 2020; Xu et al. 2021). Therefore, more information on the reproductive strategies, larval biology and life history of the seep- and/or vent-endemic species, coupled with better deep-sea hydrodynamic models, is crucial to assess the population connectivity of deep-sea macrofauna in the Northwest Pacific.

5.4 Perspectives

In this chapter, we summarized and updated the profiles of cold-seep macrofauna in the SCS. Integrative morphological and molecular analyses have resulted in the description of nine new species and plenty of new records from these areas over the last decade. However, there are still some knowledge gaps in our understanding of the biodiversity of SCS seeps: (1) as new species have been discovered with more sampling efforts, there should be still undescribed species waiting our discovery, especially those hiding under the sediment surface; (2) among the collected species, quite a few have not been identified to the species level, which hinders our understanding of their phylogenetic position and divergence history; (3) many of the collected species have not been subjected to stable isotope analysis, therefore their trophic levels remain unclear; (3) among the symbiont-hosting species, only a few (i.e. G. haimaensis, G. platifrons, A. marissinica and P. echinospica) have been subjected to detailed studies of symbiotic relationships, therefore more such studies should be conducted to reveal the diversity of symbiosis in these seep-dwelling animals, and understand how they may have exploited the ecological niches; (4) although quite a few species found on the SCS seeps are widely distributed in the Northwest Pacific, only three species (i.e., G. platifrons, S. crosnieri and B. nipponica) have been subjected to population genetic studies in order to understand the divergence and gene flow among their different populations. For the remaining species, population genetic studies should be conducted to define the biogeographic regions of deep-sea chemosynthetic ecosystems, and devise conservation plans for these ecosystems that are under increasing threats from human activities, especially mining for metal-rich sulfur deposits from vent fields and extraction of methane hydrate from cold seeps (Levin et al. 2016).