The genus Smacigastes Ivanenko & Defaye, 2004 (Harpacticoida, Copepoda) is the most primitive genus in the family Tegastidae Sars, 1904, occurring in deep-sea chemosynthetic environments, such as hydrothermal vents, cold seeps, whale falls and wood falls. Our exploration of the Onnuri Vent Field, the sixth active hydrothermal vent system in the Central Indian Ridge, resulted in the discovery of a new species in the genus Smacigastes. A detailed morphological analysis of S. pumila sp. nov. reveals that it most resembles S. barti Gollner, Ivanenko & Martínez Arbizu, 2008, described from a hydrothermal vent in the East Pacific Ridge; the new species can be distinguished from the existing species by the 8-segmented female antennule, the absence of an abexopodal seta on the antennary basis, the mandibular exopod represented by a single seta and the exopod of the first leg with five setae. This is the first record of Smacigastes in the Indian Ocean. A dichotomous key to species of the genus Smacigastes worldwide is provided.

deep sea, dichotomous key, hydrothermal vent, meiofauna, northern Central Indian Ridge

Deep-sea hydrothermal vents are special ecosystems maintained by chemosynthetic organisms that use dissolved mineral deposits (e.g. sulphide and methane) as a primary energy source, independent of solar energy (Nakamura and Takai 2015). Since the first discovery of hot springs in the Galápagos Archipelago, ecological and taxonomical information regarding hydrothermal fauna has accumulated worldwide (e.g. Hashimoto et al. 2001; Desbruyères et al. 2006; Rogers et al. 2012; Goffredi et al. 2017). Although copepods are a common and diverse group in this chemosynthetic habitat (Humes and Segonzac 1998; Heptner and Ivanenko 2002; Zeppilli et al. 2018), knowledge of this taxon is very limited due to the difficulty of sampling and because most scientific attention has been given to macro- or mega-fauna. Amongst hydrothermal copepod assemblages, dirivultid copepods belonging to the order Siphonostomatoida are the most dominant constituents (Ivanenko et al. 2011, 2012; Sarrazin et al. 2015; Lee et al. 2020); however, some studies have suggested that the order Harpacticoida might have greater species richness compared to Siphonostomatoida (Willen 2004; Cuvelier et al. 2014; Plum et al. 2017). Although fewer than 20 hydrothermal harpacticoid copepods have been documented thus far (Heptner and Ivanenko 2002; Willen 2004, 2006; Ivanenko and Defaye 2006; Plum and Martínez Arbizu 2009; Back et al. 2010; Ivanenko et al. 2011), many species still remain to be described (Willen 2004).

The family Tegastidae Sars, 1904, comprising 69 valid species in seven genera, is a harpacticoid group that is easily recognisable by the laterally-compressed and amphipod-like bodies (Plum and Martínez Arbizu 2009; Saetang and Maiphae 2015; Huys 2016; Kim et al. 2016). Although most tegastid copepods live in algal habitats, occasionally in association with other invertebrates in shallow waters (Boxshall and Halsey 2004; Wells 2007; Huys 2016), deep-sea tegastids of the genus Smacigastes Ivanenko & Defaye, 2004, as well as the species Tegastes okinawaensis Back, Huys & Lee, 2010 and T. satyrus (Claus, 1860) occur in chemosynthetic ecosystems (e.g. hydrothermal vents, cold seeps, whale falls and wood falls) (Ivanenko and Defaye 2004; Gollner et al. 2008; Plum and Martínez Arbizu 2009; Willems et al. 2009; Back et al. 2010). In hydrothermal habitats, Smacigastes species occasionally exhibit a relatively high abundance (Sarrazin et al. 2015; Plum et al. 2017) and preference for hard-substrate environments (Gollner et al. 2008). Thus far, this genus accommodates only three named species and one undescribed species: S. micheli Ivanenko & Defaye, 2004 from the Mid-Atlantic Ridge, S. barti Gollner, Ivanenko & Martínez Arbizu, 2008 from the East Pacific Ridge, S. methanophilus Plum & Martínez Arbizu, 2009 from the Gulf of Mexico and Smacigastes sp. from the Gorda Ridge (Ivanenko and Defaye 2004; Gollner et al. 2008; Plum and Martínez Arbizu 2009).

The Onnuri Vent Field (OVF), an active hydrothermal vent field in the Central Indian Ridge, was recently discovered by a research team from the Korean Institute of Ocean Science and Technology (KIOST). A survey of hydrothermal fauna in this ultramafic-hosted system resulted in the discovery of a tegastid harpacticoid that can be assigned to Smacigastes. Herein, we describe both sexes of S. pumila sp. nov. in detail and provide a dichotomous key to species of the genus Smacigastes. This is the first record of Smacigastes in the Indian Ocean.

An oceanographic expedition to the OVF, an ultramafic-hosted hydrothermal system and the sixth hydrothermal vent system discovered in the Indian Ocean, was conducted aboard the RV ISABU (15 June–3 July 2018; Fig. 1). Hydrothermal fauna was collected using a video-guided hydraulic grab (Oktopus, Germany) at a depth of 2022 m; bathymodiolin mussels of the species Bathymodiolus marisindicus Hashimoto, 2001, Bathymodiolus sp. 1 and Gigantidas vrijenhoeki Jang, Ho, Jun, Kim & Won, 2020 were dominant (Jang et al. 2020; Kim et al. 2020). To subsample meiofaunal assemblages, the collected macrofaunal animals and sediments taken by a trowel were rinsed with fresh water through a 50-μm mesh net. All subsamples were immediately fixed with a 4% formaldehyde solution. In the laboratory, meiofaunal animals were extracted by centrifugation using a Ludox HS40 at 2400 rpm (Heip et al. 1985). Tegastid harpacticoids were sorted from the extracted organisms under a stereomicroscope (Leica M165C, Germany) and were immersed in a 3% glycerine solution in a desiccator to gradually replace their content medium with glycerine. All drawings were made from the holotype and allotype with the aid of a drawing tube mounted on a differential interference contrast microscope (DIC; Leica DM2500, Germany). The dissected parts were mounted in glycerine on H-S slides. Some specimens of the new tegastid harpacticoid were prepared for examination by scanning electron microscopy (SEM; Hitachi S-4300, Japan); the detailed process for SEM was performed using the method described by Chang (2013). A series of type material was deposited in the Marine Biodiversity Institute of Korea (MABIK), Seochun, South Korea and the examined scanning electron microscopy stub was kept in the Korea Institute of Ocean Science and Technology (KIOST), Busan, South Korea. The general descriptive terminology follows that of Huys and Boxshall (1991) and the setal formula follows that of Huys et al. (1996). The scale bar in the illustrations of the new taxon is given in μm.

Figure 1. 

Map of the Onnuri Vent Field (Indian Ocean), black star showing the sampling station.

Abbreviations used in the text are: ae = aesthetasc; enp-1(-2, -3) = proximal (middle, distal) segment of endopod; exp-1(-2, -3) = proximal (middle, distal) segment of exopod; L/W = length to greatest width; P1–P6 = first to sixth thoracic leg.

There are 70 valid species, including S. pumila sp. nov., in seven genera of the family Tegastidae (Plum and Martínez Arbizu 2009; Saetang and Maiphae 2015; Huys 2016; Kim et al. 2016). The monophyly of this family is supported by the laterally-compressed, so-called “amphipod-like” body, as well as by the 1-segmented nature of both rami of P1. However, the phylogenetic relationship amongst tegastid representatives at the genus level remains somewhat unclear. For example, Kim et al. (2016) doubted the monophyly of the genus Syngastes Monard, 1924, based on the diverse morphological states of its congeners in the segmentations of the antennule and the antennary exopod, the shape of the P1 exopod, the setal armature of P2–P4 exp-1 and the male P5. Additionally, significant differences have been observed in the setation and segmentation of cephalosomal appendages within a single genus. Ivanenko and Defaye (2004) recognised differences in the number of endites in the maxillary syncoxa within the genus Tegastes Norman, 1903; only two endites are present in T. acroporanus Humes, 1981, T. harpactoides (Claus, 1863), T. paulipes Humes, 1984, T. pygmaeus Marcus, 1977, T. nanus Sars, 1904 and T. singularisaetus Marcus, 1977. In addition, some Tegastes species exhibit similar reduction of cephalosomal appendages: most Tegastes species have a 2-segmented exopod in the antenna, whereas a 1-segmented exopod is known in T. acroporanus, T. areolatus Monard, 1935, T. gemmeus Humes, 1984, T. georgei Marcus & Masry, 1970, T. harpactoides, T. paulipes, T. satyrus (Claus, 1860) and T. singularisaetus (Claus 1860, 1863; Monard 1935; Marcus and Masry 1970; Marcus, 1977; Humes 1981a; Humes 1984); most tegastid species have a tongue-like process on the palmar margin of the maxillipedal endopod distally, although this feature is absent in T. acroporanus, T. gemmeus, T. harpactoides and T. paulipes and is represented by a tubercle in T. singularisaetus. Considering these differences, at least three species (T. acroporanus, T. paulipes and T. singularisaetus) appear quite distinct from other Tegastes species. This confusion might have resulted from the relatively-simple delimitation of tegastid genera, which were traditionally distinguished, based mainly on the number of segments in P2–P4 (Sars 1904; Marcus 1977; Humes 1981a, 1984). Wells (2007) presumed that this simple classification contradicts a recent phylogenetic analysis without inspection of the characteristic of the maxilliped, the female P5 and the anterior urosomites. Only recently, studies (Ivanenko and Defaye 2004; Ivanenko et al. 2008; Huys 2016) began to focus on the structures of the genital somite complex, the female P5, the torsion of the male genital somite and the length of caudal rami as generic characteristics. The re-appraisal and application of these morphological features to the modern taxonomy of the tegastid family have been hampered by the poor and inadequate descriptions of many tegastid species in incipient studies (i.e. Claus 1860, 1863; T. Scott 1894; Thompson and A. Scott 1903; Brady 1910), which especially lack information regarding cephalosomal appendages. Reliable information concerning the mouth-part appendages has been subsequently provided by various authors (i.e. Médioni and Soyer 1967; Marcus 1977; Bartsch 1993, 1994, 1995, 1999; Humes 1981a, b, 1984). A re-appraisal and cladistic analysis, based on the morphology of cephalosomal appendages, would help to clarify the phylogenetic relationship of tegastid species. Further revisional works should re-examine the specimens of older species with outdated morphological descriptions.

According to the ground pattern of Tegastidae proposed by Seifried (2003), the palmar margin of the maxillipedal basis of tegastid species has one proximal short seta or spine and one distal pad-like sensory element, which has been variously described as a mushroom-like stalked structure by Wells (2007) a scaphoid by Lang (1965), a tongue-like process by Bartsch (1994, 1995, 1999) and a spinulose pad by Huys et al. (1996). Wells (2007) suggested that the latter element, along with rows of spinules or setules on the proximal part, enhances the grasping ability of the maxilliped in tegastid species. The proximal short seta of the maxillipedal basis has been observed in most tegastid species. However, Syngastes species exhibit a peculiar form of tubercle or a cylindrical (button-like) process, instead of the proximal seta in the position where the proximal seta should be; an exception is Syngastes serratus Lang, 1965, which – like Smacigastes methanophilus – has no proximal elements on the maxillipedal basis. We presume that these elements are homologous structures, based on their position. It is likely that this morphological change increases the grasping ability, aiding Syngastes species in the attachment to algal substrata. Most Syngastes species are typically associated with macroalgae and seagrass in shallow waters, subject to more challenging environmental changes (such as rough waves) than the deep-sea-dwelling Smacigastes species. In contrast, the loss of the distal pad-like process, as well as a reduction of cephalosomal appendages (as mentioned above), are sometimes observed in species that have symbiotic associations with other invertebrates, including Aglaogastes cnidicus (Humes, 1981) (hydroid), T. acroporanus (scleractinian coral), T. gemmeus (scleractinian coral) and T. paulipes (scleractinian coral; Humes 1981a, 1984; Huys 2016).

T. Scott (1894) described a tegastid species as Amymone andrewi (= Tegastes andrewi) from São Thomé Island in the Gulf of Guinea, but his insufficient description and illustrations are limited to the habitus and part of the cephalosomal appendages. Although complete information regarding the thoracic legs is unavailable, this species has been conventionally assigned to the genus Tegastes (Wells 2007). However, the structure of the maxilliped provides a hint regarding the taxonomic status of T. andrewi. The palmar margin of the endopod has a proximal tubercle, which could be considered a powerful autapomorphy of the genus Syngastes (see T. Scott 1894: plate 10, Fig. 1); this aspect indicates a close relationship between T. andrewi and Syngastes species. Therefore, we have removed this species from the genus Tegastes and tentatively transferred it to the genus Syngastes as Syngastes andrewi (T. Scott, 1894) comb. nov., pending a redescription.

Ivanenko and Defaye (2004) established the deep-sea genus Smacigastes for S. micheli and assumed this genus to be the most primitive group in the family Tegastidae, based on the following distinct plesiomorphic features: (1) the integument of body and appendages is weakly chitinised; (2) the antennules of females and males are 8- and 10-segmented, respectively; (3) both rami of P2–P4 are 3-segmented, whereas the three subsequently described species (S. barti, S. methanophilus and S. pumila sp. nov.) have 2-segmented exopods in P2–P3; (4) the urosome is composed of five urosomites, including a genital double-somite in both sexes; (5) the caudal rami of both sexes are elongate, approximately 3-fold longer than their width; and (6) the female P6 with two elements is present and observable. Comparison of the morphology of cephalosomal appendages of Smacigastes with that of other tegastid genera also supports their assumption, whereby Smacigastes retains the following plesiomorphic states of tegastid species: (1) the antennary basis of both S. barti and S. micheli has an abexopodal seta, which has not been reported in other tegastid species; (2) the distal endopodal segment of the antenna in all Smacigastes species has a lateral armature composed of four setae, whereas three setae are present in Feregastes wellensi Fiers, 1986, two setae are present in most tegastid species and no setae are present in Arawella alexandri Cottarelli & Baldari, 1987; (3) the endopod of the mandible has a lateral seta in all Smacigastes species, as well as in Arawella alexandri, Parategastes sphaericus (Claus, 1863), Syngastes foveatus Bartsch, 1994, Syngastes pseudofoveatus Kim, Jung & Yoon, 2016, T. falcatus (Norman, 1869), T. fernandici Pallares, 1979, T. knoepffleri Médioni & Soyer, 1967, T. okinawaensis and T. pygmaeus, but it is absent in the other tegastid species; and (4) the exopodal lobe of the mandible of Smacigastes micheli has three setae, while other tegastid species have 0–2 setae (Sars 1904; Médioni and Soyer 1967; Marcus 1977; Pallares 1979; Fiers 1986; Cottarelli and Baldari 1987; Bartsch 1994; Ivanenko et al. 2008; Back et al. 2010; Kim et al. 2016). Ivanenko et al. (2008) described the copepodid development of T. falcatus. The maxillule of the copepod phase I has a 1-segmented exopod with three setae, but this segment is reduced into a seta in the adult. Considering this feature, the 1-segmented exopod of the maxillule in Smacigastes is more primitive than the single seta present in Aglaogastes cnidicus, F. wellensi, P. conexus Humes, 1984, P. sphaericus, T. falcatus, T. gemmeus, T. paulipes and T. singularisaetus; moreover, the exopod is absent in Arawella alexandri, P. herteli Jakobi, 1953 and T. acroporanus (Sars 1904; Jakobi 1953; Marcus 1977; Humes 1981a, b, 1984; Fiers 1986; Cottarelli and Baldari 1987; Ivanenko et al. 2008).

Amongst Smacigastes species, S. micheli is the most primitive, based on the presence of three setae on the mandibular exopodal lobe; additionally, both rami of P2–P4 have three segments. Conversely, S. barti exhibits more derived conditions within the genus, in terms of the following features: (1) the female antennules are 7-segmented (vs. 8-segmented); (2) the exopodal lobe of the mandibular palp is absent (vs. represented by 1–3 setae); (3) the endopod of the maxillule is represented by a single seta (vs. 2–3 setae); (4) the basis of the P1 has no inner seta (vs. setae are present in S. micheli and S. pumila sp. nov.); and (5) the exopod of the P1 has four setae (vs. five setae; Table 1).

Former records of Smacigastes were from the Atlantic and Pacific Oceans. Our discovery of S. pumila sp. nov. from the Central Indian Ridge extends the distribution area of Smacigastes. All representatives of Smacigastes have been found from deep-sea chemosynthetic habitats, such as hydrothermal vents (S. barti, S. micheli and S. pumila sp. nov.), cold seeps (S. methanophilus) and wood falls (undescribed Smacigastes species) (Gollner et al. 2008; Plum and Martínez Arbizu 2009). Hydrothermal vent fluids with high temperature cause the temporal gradients of the surrounding seawater (maximum temperature are usually less than 50 °C) in the vent fauna (Govenar 2010). Gollner et al. (2008) suggested that S. barti has reduced tolerance to high temperatures and Ivanenko et al. (2012) found out that the abundance of S. micheli was relatively higher in the low temperatures (4.8–7.5 °C). The OVF, the type locality of S. pumila sp. nov., is also known to be an ultramafic-hosted hydrothermal system with the low temperatures (Kim et al. 2020). Therefore, Smacigastes species seem to prefer relatively low temperatures. The occurrence of S. pumila sp. nov. from the OVF dominated by bathymodiolin mussels reflects their preference of hard-substrate nutrient-rich environment as suggested by Gollner et al. (2008). It seems that mussel shells provide a harbour for filamentous bacteria that are probably food sources of Smacigastes species as suggested by Ivanenko et al. (2012).

The authors thank the captain and crews of the RV ISABU for their support and assistance with the sample collection. We also express our gratitude to editor Dr Kay Van Damme and two reviewers, Dr Viatcheslav N. Ivanenko and Dr Kai Horst George, for their helpful advice and comments on the manuscript. This research work was conducted by the project ‘Understanding the deep-sea biosphere on seafloor hydrothermal vents in the Indian Ridge’ of the Korea Institute of Marine Science and Technology Promotion (KIMST) funded by Ministry of Oceans and Fisheries, Kores (No. 20170411) and by KIOST (PM61740). This work was also supported by a research programme of KIMST (No. 20170431) and by a grant (2018R1A6A3A01012703) of the National Research Foundation of South Korea (NRF) to JG Kim.