Research Article |
Corresponding author: Haibin Zhang ( hzhang@idsse.ac.cn ) Academic editor: Didier Vanden Spiegel
© 2024 Yunlu Xiao, Haibin Zhang.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Xiao Y, Zhang H (2024) Three new species and one new record of Deimatidae (Echinodermata, Holothuroidea, Synallactida) discovered in the South China Sea and the Mariana fore-arc area using integrative taxonomic methods. ZooKeys 1195: 309-335. https://doi.org/10.3897/zookeys.1195.115913
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Deep-sea holothurian specimens were collected during five scientific expeditions (2018–2023) using the submersible vehicle ‘Shenhaiyongshi’. Our examination of specimens of Deimatidae from the South China Sea and the Mariana fore-arc area revealed three new species, which were described as Oneirophanta idsseica sp. nov., Oneirophanta brunneannulata sp. nov., and Oneirophanta lucerna sp. nov. These species were distinguished from each other and from congeners by the arrangement, and number of ventrolateral tube feet and ossicle types. We also reported Oneirophanta mutabilis mutabilis Théel, 1879 for the first time from the Mariana fore-arc area, and we recorded Deima validum validum for the second time from the South China Sea. The taxonomy of these new species and new records is discussed, and a phylogenetic analysis based on a concatenated dataset of 16S and COI genes was conducted. Additionally, the inter- and intraspecific genetic divergences we calculated among deimatid species. The results support the assignment of these new species to the genus Oneirophanta and their separation from congeners. A description of the main morphological characters of Oneirophanta species is also provided. The data were collected from geographically diverse areas and suggest that species of Deimatidae were abundant in the Pacific Ocean and occupied a wide range of depths.
COI, deep-sea, morphology, Oneirophanta, phylogeny, sea cucumber, SEM, taxonomy
Echinoderms are abundant in Chinese seas, and the South China Sea has more species than the Yellow Sea and the East China Sea (
Holothurians are the dominant epibenthic invertebrate taxon in many areas of the deep sea, and they account for 90% of that ecosystem’s biomass (
The family Deimatidae formerly belonged in the order Elasipodida Théel, 1882, but was later transferred to the order Aspidochirotida by
In addition, we present a morphological description of Deima validum validum Théel, 1879, which was recorded for the second time in the South China Sea; the present specimens show some variations compared with specimens that were recorded previously. Our study provides comprehensive a description of morphological characters, an assessment of intraspecific divergence between the new species and all other known species, and more molecular details that may be useful for further studies of the phylogeny and diversity of the family Deimatidae.
Specimens were collected from the South China Sea and the Mariana fore-arc area (Fig.
The specimens of each species were identified using a variety of original descriptions and literature (
Total genomic DNA was extracted from small pieces of 20–30 mg holothurian muscle tissue using a TIANamp Marine Animals DNA Kit (TianGen, Beijing), according to the manufacturer’s instructions. Mitochondrial cytochrome c oxidase I (COI) and 16S rRNA were generated for various specimens using the primers and methods outlined in
Two partial sequences (COI and 16S) were obtained from specimens and were deposited in GenBank (Table
Species | GenBank accession number | Reference | |
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16S | COI | ||
Deimatidae | |||
Orphnurgus glaber | KX856746 | KX874361 |
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Deima validum | KX856744 | KX874364 |
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Deima validum validum SY155-HS01 | N/A | OR413734 | this study |
Deima validum validum SY84-HS02 | OR658899 | OR413743 | this study |
Oneirophanta setigera | KX856745 | KX874363 |
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Oneirophanta stet. CCZ_100 | N/A | ON400706 |
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Oneirophanta cf. mutabilis | ON406619 | ON400724 |
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Oneirophanta idsseica sp nov. SY86-HS01 | OR658900 | OR413744 | this study |
Oneirophanta idsseica sp. nov. SY84-HS01 | OR658898 | OR413742 | this study |
Oneirophanta idsseica sp. nov. SY283-HS01 | OR658902 | OR413737 | this study |
Oneirophanta brunneannulata sp. nov. SY157-HS01 | OR658901 | OR413733 | this study |
Oneirophanta mutabilis SY310-HS01 | OR658897 | OR413735 | this study |
Oneirophanta lucerna sp. nov. SY529-HS02 | OR658906 | OR413738 | this study |
Oneirophanta lucerna sp. nov. SY530-HS01 | OR658903 | OR413739 | this study |
Oneirophanta lucerna sp. nov. SY530-HS02 | OR658904 | OR413740 | this study |
Oneirophanta lucerna sp. nov. SY530-HS03 | OR658905 | OR413741 | this study |
Outgroups | |||
Apostichopus californicus | DQ777096 | HM542319 |
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Apostichopus parvimensis | KX856750 | KX874373 |
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Sequence alignments were generated using MAFFT7 (
Order Synallactida Miller, Kerr, Paulay, Reich, Wilson, Carvajal & Rouse, 2017
Family Deimatidae Théel, 1882
Genus Oneirophanta Théel, 1879
Oneirophanta
stet. CCZ_100,
Holotype. IDSSE-2018-0612-HS01, collected from the Xisha Trough of the South China Sea, station SY86-HS01 (18°16.11'N, 113°25.32'E), depth 2985 m, 12 Jun. 2018, preserved in absolute alcohol. Paratypes. Two specimens. IDSSE-2018-0531-HS01, collected from the Xisha Trough of the South China Sea, station SY84-HS01 (18°2.70'N, 114°3.51'E), depth 3156 m, 31 May 2018, preserved at -80 °C. IDSSE-2020-0917-HS01, collected from the northern slope of the South China Sea, station SY283-HS01 (17°23.20'N, 115°32.32'E), depth 3806 m, 17 Sep. 2020, preserved in absolute alcohol.
In the Xisha Trough, which is located in the northern slope of the South China Sea, depth 2985 m.
Body elongated and cylindrical, color yellowish-white. Tentacles 15. Ventrolateral tube feet up to 40–50 pairs, in alternating two or three rows. Dorsal papillae 18–20 on each side, in single rows. Ventrolateral papillae 9–12 on each side, in single rows. Midventral tube feet two and rudimentary. Dorsal deposits irregular perforated plates and varying types of crosses. Perforated plates and crosses with open ramifications ventrally. Papillae deposits slender and sturdy rods with spatulated ends, and crosses with open ramifications. Spatulated rods and irregular deposits in tube feet. Sturdy spatulated rods in tentacles.
External morphology. Body elongated and cylindrical, ventrum flattened. 29 cm long and 9 cm wide before fixation (Fig.
Ossicle morphology. Dorsal deposits contain (1) perforated plates with open ramifications (Fig.
SEM images of different tissues from Oneirophanta idsseica sp. nov. (Holotype: IDSSE-2018-0612-HS01) A1–A10 dorsal body wall B1–B10 papillae C tentacles D1–D4 tube feet E1–E5 ventral body wall. Scale bars: 50 μm (A1, A2, A7, B3, B4, D3, D4, E4); 100 μm (A3–A6, A8, A10, B2, B5, B6, E3, E5); 300 μm (A9, B1, B7–B10, C, D1, D2, E1, E2).
Consists of IDSSE and the Latin suffix icus (belonging to), to honor IDSSE’s contributions and efforts to the field of deep-sea exploration.
A seamount in APEI 4, Clarion Clipperton Zone; Xisha Trough, the northern slope of the South China Sea, at depths of 2985–3806 m.
Oneirophanta idsseica sp. nov. is characterized by the arrangement of ventrolateral tube feet in two or three rows that number up to 40–50 pairs with distinctive cross-types in dorsal deposits. O. idsseica sp. nov. is distinct from Oneirophanta setigera (
The phylogenetic trees showed that O. idsseica sp. nov., together with an unnamed species (Oneirophanta stet. CCZ_100, see below), formed a sister group that included Oneirophanta cf. mutabilis and O. mutabilis. From a morphological point of view, O. idsseica sp. nov. mostly resembled O. stet. CCZ_100 with ventrolateral tube feet arranged in two or three rows, two rudimentary midventral tube feet, spatulated crosses and small, irregular perforated plates on dorsum, and crosses with open ramifications in different stages of development on the ventrum. From a molecular point of view, the COI pairwise distance between O. idsseica sp. nov. and O. stet. CCZ_100 was 0.6% (Suppl. material
Holotype. IDSSE-2018-0612-HS01, collected from the continental slope of the South China Sea, station SY157-HS01 (18°51.18'N, 114°24'E), depth 1340 m, 1 Jul. 2019, preserved in -80 °C
On the continental slope of the South China Sea, depth 1340 m.
Body elongated, color reddish brown, with darker tentacles and tube feet. Mouth and anus ventral. Tentacle 20. Ventrolateral tube feet ~ 37 pairs, each tube foot end with a brown ring, arranged in alternating three rows, bilateral symmetry. Dorsal papillae 23–26 on each body side, arranged in single rows. Ventrolateral papillae 9–11 on each body side. Midventral tube feet two and rudimentary. Deposits perforated plates, rods of varying shapes and few spatulated crosses.
External morphology. Body elongated, dorsum convex, ventrum flattened. 20 cm long, and 5 cm wide before fixation (Fig.
Ossicle morphology. Dorsal deposits only robust perforated plates present (Fig.
The specific epithet brunneannulata in Latin means brown rings. It is here used as a noun in apposition and refers to the distinctive brown rings around the tube feet.
Only in the type locality.
Oneirophanta brunneannulata sp. nov. differs from other species in the genus in possessing brown rings at the end of tube feet that are arranged in three rows along ventrolateral radii. O. brunneannulata sp. nov. is relatively similar to O. mutabilis in possession of plates and spatulated rods, but there are differences: (1) different diameters of perforated plates, 0.6–1.1 mm in O. brunneannulata sp. nov., but 2–3 mm in O. mutabilis, and some perforated plates in O. brunneannulata sp. nov. possess a central apophysis. (2) different types of deposits in tube feet, O. brunneannulata sp. nov. has various forms of spatulated rods and a few spindle-shaped rods, but lacks perforated plates, and there are perforated plates in addition to sturdy and spatulated rods in O. mutabilis. O. brunneannulata sp. nov. differs from O. setigera in having perforated plates on the dorsum and the ventrum, lacked spatulated crosses, and had a large number of tube feet that were arranged in three rows. Larger central perforations on perforated plates were in papillae, and the presence of spatulated rods and papillae were arranged in single rows along the dorsal radius (double rows along dorsal radius in O. conservata) distinguished O. brunneannulata sp. nov. from O. conservata (Table
Characteristics | O. idsseica sp. nov. | O. brunneannulata sp. nov. | O. lucerna sp. nov. | O. conservata | O. setigera | O. mutabilis mutabilis | O. mutabilis affinis |
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Tentacle number | 15 | 20 | 19 or 20 | Only eight founded | 15–20 | 18–20 | 18–20 |
Ventrolateral tube feet number and arrangement | 40–50 pairs, in alternating two or three rows | ~ 37 pairs, in alternating three rows | 11–14 on each side, in single rows | 33–34 on each side, in two rows | 16–30 on each side, in alter-nating double rows | 8–28 (36), in alterna-ting double rows | 15–20 (44), – |
Dorsal papillae number and arrangement | 18–20 on each side, in single rows | 23–26 on each body side, in single rows | 15–27 on each body side, in regular single rows | 30, in double rows | 12–32, in irregular double rows | 4–19, in single rows | 5–35, in single or double rows |
Ventrolateral papillae number and arrangement | 9–12 on each side, in single rows | 9–11, in single rows | 7–10, in single rows | 13, in two rows | 9–17, – | 4–17, – | 5–11, – |
Midventral tube feet number and arrangement | Two and rudimentary, one positioned in the front third of the body, the other positioned in the back third of the body | Two, rudimentary, one placed on half the body, the other placed on a rear quarter of the body | Two and rudimentary, one placed on half the body, the other on a rear quarter of the body | 12, placed through-out the entire length of this radius, sometimes in pairs | 0–6, in front of the anus | 0–4, pre-anal | 3–9, usually one pair placed pre-anal |
Dorsal Deposit | Perforated plates with open ramifications and crosses with dichotomously ramified ends or irregular, and spatulated rods | Perforated plates, 0.6–1.1 mm in diameter, some with irregular central apophysis | Spatulated crosses, spinous rods with branched spines, spatulated rods up to 1 mm | Perforated plates, some in the developmental stage, rods with slightly thorny surfaces, pointed or bifid ends occasionally | Spatulated crosses, 1.1–3 mm | Perforated plates, 2–3 mm in diameter, bearing several small, vertical spines, with a rather slender mesh-work | Robust and rather small, vertical spines, often irregularly shaped due to elongation of the primary rod |
Ventral | Perforated plates and crosses with open ramifications | Numerous irregular broken deposits, amorphous shaped | Spinous rods and spatulated crosses with arms twice divided | – | Spatulated crosses, 0.2–2.3 mm | Vary more, less well-developed, and less irregular than dorsal ones | – |
Papillae | Slender or sturdy rods, crosses with open ramifications, some bearing 2–3 processes | Perforated plates with 2–4 large central holes, robust spatulated rods and few spatulated crosses | Spinous rods and spatulated rods | Spatulated rods | Perforated plates only | Perforated plates, small, sturdy and spatulated rods | |
Tube feet | Mainly robust spatulated rods and irregular deposits | Smooth spindle-shaped rods, slender rods with dichotomously ramified ends, sturdy spatulated rods with rudimentary or enlarged ends | Spinous rods of two types, one irregularly shaped, the other with few regularly distri-buted spines, sturdy spatulated rods with perforated extremities that occasionally bifurcated | – | Perforated plates | Sturdy and spatulated rods | |
Tentacle | Sturdy spatulated rods | Slender and sturdy rods with open ramifications | – | Irregularly placed and stout rods, somewhat branched | Clusters of rod-shaped spicules | ||
Data source |
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This study | This study |
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Holotype. IDSSE-2023-0208-HS02, northern slope of the South China Sea, station SY530-HS02 (16°28.60'N, 110°18'E), depth 1389 m, 8 Feb. 2023, preserved in absolute alcohol. Paratypes. Three specimens. IDSSE-2023-0204-HS02, northern slope of the South China Sea, station SY529-HS02 (16°28.20'N, 110°43'E), depth 1393 m, 4 Feb. 2023, preserved in absolute alcohol. IDSSE-2023-0208-HS01, northern slope of the South China Sea, station SY530-HS01 (16°28.30'N, 110°43'E), depth 1389 m, 8 Feb. 2023, preserved in absolute alcohol. IDSSE-2023-0208-HS03, northern slope of the South China Sea, station SY530-HS03 (16°28.18'N, 110°43'E), depth 1392 m, 8 Feb. 2023, preserved in absolute alcohol.
Northern slope of the South China Sea, depth 1389 m.
Body elongated, skin smooth, color orange in vivo. Mouth anteroventral, anus posteroventral. Tentacle 19 or 20. Ventrolateral tube feet 11–14 on each body side, arranged in single rows. Midventral tube feet two and rudimentary. Dorsal papillae 15–27 on each side, placed in single rows along dorsal radius. Ventrolateral papillae 7–10 on each side, arranged in single rows. Dorsal deposits spatulated crosses, spatulated rods, and widely scattered spinous rods with branched spines. Papillae deposits with spinous rods and spatulated rods. Spatulated crosses with the arms twice divided and two types of spinous rods are in ventrum. Spinous rods and sturdy spatulated rods with open ramifications in tentacles and tube feet.
External morphology. Body elongated, dorsum inflated, ventrum flattened, slightly narrowed anteriorly (Fig.
Ossicle morphology. Dorsal deposits contain spatulated crosses, spinous rods and spatulated rods. Spinous rods with irregular spines, 0.1–0.2 mm in length (Fig.
The species was named after the Latin word lucerna to commemorate the traditional Chinese Lantern Festival, which was relatively close to the time these specimens were collected.
Northern slope of the South China Sea, depths of 1389–1393 m.
The new species conformed to the genus Oneirophanta characterized by uncontracted the tentacles, the absence of oral papillae and tentacle discs without ramified processes. Oneirophanta lucerna sp. nov. differed from other species of Oneirophanta in possessing highly variable shaped spinous rods and ventrolateral tube feet that are only arranged in single rows, whereas, in other species (Table
Oneirophanta mutabilis
Théel, 1879: 6–7, figs 4–6;
Oneirophanta mutabilis mutabilis
Théel:
Oneirophanta alternata
R. Perrier, 1900: 117–118; R.
Oneirophanta alternata var. talismani R. Perrier, 1902: 386–388, fig. 6.
One specimen. IDSSE-2020-1203-HS01, in the Mariana fore-arc area, western Pacific Ocean, station SY310-HS01 (11°41.42'N, 140°58.56'E), depth 3394 m, 3 Dec. 2020, preserved in absolute alcohol.
External morphology. Body cylindrical, nearly equal in width throughout the whole length and tapering anteriorly. 15 cm long and 4.5 cm wide after fixation with 95% alcohol for several days (Fig.
Ossicle morphology. The body wall and papillae with perforated plates (Fig.
Cosmopolitan, depth 2515–6000 m (
Oneirophanta mutabilis was first described west of the Crozet Islands (H.M.S. Challenger station 146: 46°46'S, 45°31'E) at depths of 2514 m (
Genus Deima Théel, 1879
Deima validum
Théel, 1879: 5, figs 36–38;
Deima validum validum:
Deima fastosum
Théel, 1879: 5–6, figs 1–3;
Deima blakei
Théel, 1886b: 1–2, figs 1, 2;
Deima atlanticum Hérouard, 1898: 88–89, figs 1, 2.
Deima mosaicum Ohshima, 1915: 233–234.
Two specimens. IDSSE-2019-0630-HS01, collected from the northern slope of the South China Sea, station SY155-HS01(17°43'N, 114°13'E), depth 3451 m, 30 Jun. 2019, preserved in absolute alcohol. IDSSE-2018-0531-HS02, collected from the Xisha Trough of the South China Sea, station SY84-HS02 (18°2'N, 114°5'E), depth 3404 m, 31 May 2018, preserved at -80 °C.
External morphology. Body ovate, dorsal vaulted, ventral flattened. 9–10 cm long and average 5.5 cm wide in vivo. Skin rigid, body wall brittle and easily broken. Color orange in vivo (Fig.
Ossicle morphology. Basal layer and several additional layers amount in the center of the perforated plates on the body wall and dorsal papillae, in diameter 0.6–1.8 mm (Fig.
This subspecies probably has a cosmopolitan distribution, except for the Arctic and Southern Ocean, at depths of 724–5426 m (
Deima validum was first described by
The two specimens examined here are consistent with the diagnosis of subspecies D. v. validum as described in detail by
Only in the Bay of Bengal (depth 1224–3365 m) did the development of additional layers of meshwork increase progressively with depth. In this research, high-knobbed plates were present in the abyssal South China Sea specimens (depth > 3000 m), but they were absent from the South China Sea specimens first reported (depth 1100 m) by
The inter- and intraspecific genetic divergences of the COI gene were calculated to calculate the genetic distances in Deimatidae (Suppl. material
In total, 11 COI sequences and 10 16S sequences were deposited into GenBank (Table
Maximum likelihood (ML) and Bayesian inference (BI) trees based on concatenated 16S-COI sequences showing phylogenetic relationships among deimatid species. The new sequences provided in this study are in bold A ML tree, with bootstrap replications labeled B BI tree, with posterior probability labeled.
The phylogenetic relationships of Deimatidae clustered into three portions and were consistent with the traditional classification system (Fig.
Both the morphology and molecular phylogenetic analyses supported the assignment of the three new species to the genus Oneirophanta. The external morphological characteristics in Oneirophanta species were quite similar to those in Orphnurgus, but Oneirophanta never has tentacle discs with ramified processes, and they usually have rounded knobs on the margin. The three new species described in this study conformed to this feature.
Oneirophanta brunneannulata sp. nov., Oneirophanta idsseica sp. nov. and Oneirophanta lucerna sp. nov. can be separated from other congeners by ossicle types, the arrangement and the number of dorsal papillae and tube feet. The separations were confirmed by the p-distance analyses, which showed that the uncorrected p-distance for the COI among O. brunneannulata sp. nov. and other congeners was 8.2–13.1%; among O. idsseica sp. nov. and other congeners was 8.2–14.1%, and among O. lucerna sp. nov. and other congeners was 12.1–14.8%. These divergences were much higher than the known intraspecific variation in Oneirophanta spp. (0–0.6%) (Suppl. material
The phylogenetic trees (Fig.
There are a total of three genera and 16 species in the family Deimatidae, which include the three species that we described here. To date, 11 species of Deimatidae have been discovered in the deep water of the Pacific Ocean. Deima only includes one species: Deima validum, which occurs worldwide at depths of 724–5426 m. Nine species of Orphnurgus are accepted, with five species recorded from the Pacific: Orphnurgus dorisae Pawson, 2002 from the southern Pacific Ocean (New Zealand), Orphnurgus glaber Walsh, 1891 from the central and western Pacific Ocean, Orphnurgus protectus (Sluiter 1901) and Orphnurgus bacillus Cherbonnier & Féral, 1981 from the western Pacific Ocean (Celebes Strait and Philippines), and Orphnurgus vitreus (
Based on their distribution, deimatid holothurians are abundant in the Pacific Ocean and inhabit a wide range of depths (174–6000 m). Future expeditions to the Pacific zone may discover even more species, and more research is needed to evaluate the species diversity and geographic distribution of these deep-sea holothurians.
The authors would like to sincerely thank the crew of the vessel ‘Tansuo 1’ and the ‘Shenhaiyongshi’ HOV team for their assistance during the survey. We appreciate the members of the marine ecology and evolutionary biology laboratory at the Institute of Deep-sea Science and Engineering, Chinese Academy of Sciences, for photographing freshly collected specimens on board. We are also extremely grateful to Professor Shenghua Mei from Deep-sea Extreme Environment Simulation Research Laboratory for electron microscope support and Zhi Zheng and Mengjun Xiong for their help in taking SEM pictures of ossicles.
The authors have declared that no competing interests exist.
No ethical statement was reported.
This study was supported by the National Key Research and Development Program of China (2023YFC2809300, 2016YFC0304905), the Major scientific and technological projects of Hainan Province (ZDKJ2021036), Strategic Priority Research Program of the Chinese Academy of Sciences (
Yunlu Xiao conceived and designed this project, performed morphological examination and description, conducted molecular analyses, and wrote or reviewed drafts of the paper. Haibin Zhang conceived and designed this project, reviewed and edited drafts of the paper and approved the final draft.
Haibin Zhang https://orcid.org/0000-0001-5429-9851
All of the data that support the findings of this study are available in the main text or Supplementary Information.
Estimates of p-distances of the COI gene among deimatid species and studied sequences
Data type: docx