Research Article |
Corresponding author: Xue-Bao He ( hexuebao@tio.org.cn ) Academic editor: Christopher Glasby
© 2022 Jun-Hui Lin, Ya-Qin Huang, Qian-Yong Liang, Xue-Bao He.
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:
Lin J-H, Huang Y-Q, Liang Q-Y, He X-B (2022) A new eyeless species of Nereis (Annelida, Nereididae) from deep-sea sediments of the northern South China Sea. ZooKeys 1134: 23-37. https://doi.org/10.3897/zookeys.1134.94198
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A variety of nereidid species have been reported from the South China Sea, although little is known about the deep-sea species in this area. Recently, two specimens belonging to a novel nereidid polychaete were collected from a sedimentary habitat during an environmental survey to a deep-sea basin where cold seeps occur. This new species, Nereis tricirrata sp. nov., is described herein, based on morphological and molecular analyses. The most noteworthy feature is the absence of eyes on the prostomium; it can be distinguished from other eyeless Nereis species by the arrangement of conical paragnaths on the pharynx, the nature of homogomph falcigers and the shape of notopodial lobes in posterior chaetigers. The reconstructed phylogenetic tree, using concatenated sequences of mtCOI, 16S, and 18S rRNA, showed that all Nereis species included in this study form a monophyletic clade with full support. The mtCOI-based interspecific comparisons revealed a high genetic divergence (23.1%–37.3% K2P) from four-eyed Nereis species with the available sequences. This is the first record of an eyeless Nereis species in the South China Sea.
Nereidiformia, phylogeny, polychaete, systematics, taxonomy
Members of the annelid family Nereididae are commonly seen in marine and brackish benthic communities. The family is among the most diverse taxa groups, with 709 nominal species in 43 genera (
The South China Sea (SCS) is the largest marginal sea in the western Pacific, a biogeographic region which harbors diverse marine fauna (
During an environmental survey to a deep-sea basin of the northern South China Sea in 2019, where cold seeps occur, two interesting nereidid specimens without prostomial eyes were collected from a sedimentary habitat. In this study, they are described and illustrated as a new species, Nereis tricirrata sp. nov., based on morphological and molecular analyses. This is the first record of an eyeless Nereis species in the South China Sea.
In June 2019, sediment samples were collected at two sites in a deep-sea basin of the northern South China Sea (Fig.
In the laboratory, the specimens were examined using a Leica MZ9.5 optical stereoscope and a Leica DM6B compound microscope. Several parapodia from anterior, middle, and posterior parts of the holotype were dissected and mounted on slides for observation. Light photographs were taken under a Leica M205A stereoscope, equipped with a DFC 550 digital camera. The shape of the chaetae was observed and photographed under a Leica compound microscope (DM6B). Plates were prepared using the software Adobe Photoshop CS5. The terminology of parapodial structures used in this study follows
The total genomic DNA was extracted from the ethanol-preserved tissue sample of the holotype using a Transgen Micro Genomic DNA EE 181 Kit (Transgen, Beijing, China), following the manufacturer’s protocol. Polymerase chain reactions (PCRs) were conducted to amplify partial sequences of mitochondrial (mtCOI, 16S) and nuclear (18S, H3) genes using primer sets as shown in Table
Gene | Primer name | Sequence (5' to 3') | Reference |
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COI | LCO 1490 | GGTCAACAAATCATAAAGATATTGG |
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HCO 2198 | TAAACTTCAGGGTGACCAAAAAATCA |
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16S | 16SarL | CGCCTGTTTAACAAAAACAT |
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16SbrH | CCGGTCTGAACTCAGATCACGT |
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H3 | aF | ATGGCTCGTACCAAGCAGAC |
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aR | ATATCCTTRGGCATRATRGTGAC |
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18S1 | F | GCTGTATGTACTGTGAAACTGCG |
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R | GGAATTACCGCGGCTGCTGGCACC |
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18S2 | F | GTTCGATTCCGGAGAGGGAGCCT |
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R | GTTTCGGCCTTGCGACTATACTT |
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18S3 | F | ACTGCGAAAGCATTTGCCAAGAGT |
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R | CACCTACGGAAACCTTGTTACGAC |
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For phylogenetic analyses, the sequences of related genera of Nereididae were downloaded from GenBank, as well as species from Hesionidae (sister to Nereididae as verified by
Order Phyllodocida Dales, 1962
Nereis pelagica Linnaeus, 1758.
(after
Holotype : TIO-BTS-Poly-137, complete, northern South China Sea, (17°33'N, 111°9'E), 1766 m depth, coll. Jun-Hui Lin, 16 June 2019. Paratype: TIO-BTS-Poly-138, incomplete, northern South China Sea, (18°26'N, 112°26'E), 1157 m depth, coll. Jun-Hui Lin, 21 June 2019.
The new species is characterized by: (1) absence of eyes on the prostomium; (2) possession of three anal cirri instead of two on the pygidium; (3) few paragnaths on both rings of the pharynx; (4) notopodial and neuropodial ligules acutely conical; and (5) homogomph falcigers in posterior notopodia with several coarse teeth.
Holotype complete but broken into two fragments. Body tapering posteriorly. Anterior fragment 35.27 mm long for 44 chaetigers, remaining posterior fragment 7.28 mm long for 15 chaetigers (including regenerated segments), maximum width 2.1 mm (excluding parapodia) at chaetiger 7. Paratype incomplete, broken into three fragments with 45 chaetigers, 12 chaetigers and 7 chaetigers, respectively. Body in formalin light brown. Preserved specimens without pigmentation (Fig.
Nereis tricirrata sp. nov., holotype (TIO-BTS-Poly-137) A anterior fragment, lateral view B anterior end, dorsal view C posterior end, dorsal view, intersegmental grooves of regenerated segments have been outlined with white lines D–H right parapodia (chaetigers 1, 5, 20, 40, posterior end), posterior view. Scale bars: 1 mm (A–C); 0.5 mm (D–H).
Prostomium pentagonal and slightly longer than wide, with one pair of digitiform frontal antennae (Fig.
Peristomium apodous, 1.5 times as long as chaetiger 1. Four pairs of tentacular cirri slender, distally tapered (Fig.
Pharynx dissected, with dark brown jaws, distally curved, each with 15 blunt teeth on cutting edge. Small conical paragnaths sparse on both rings, arranged as follows: Area I = 0; II = 4 cones in a row; III = 0; IV = 2; V = 0; VI = 1; VII-VII = 2.
First two chaetigers uniramous, remaining ones biramous. Uniramous chaetigers with acutely conical dorsal ligules, subequal in length and of similar shape to ventral ligule (Fig.
Notopodia of biramous chaetigers with dorsal and ventral ligules, without notopodial prechaetal lobes. Notopodial dorsal ligules acutely conical (Fig.
Neuropodia of biramous chaetigers with neuroacicular ligules subtriangular, postchaetal lobes rounded (Fig.
In anterior parapodia, notochaetae with four homogomph spinigers (Fig.
Nereis tricirrata sp. nov., holotype and paratype A chaetiger 5, notochaetae B, C chaetiger 5, neurochaetae D chaetiger 20, notochaetae E, F chaetiger 20, neurochaetae G chaetiger 40, notochaetae H, I chaetiger 40, neurochaetae J posterior end, notochaetae (from paratype, as blades of notochaetae missing in the posterior fragment of holotype) K, L posterior end, neurochaetae. Abbreviations: HoS, homogomph spiniger; HoF, homogomph falciger; HeS, heterogomph spiniger; HeF, heterogomph falciger; DoF, dorsal fascicle; VeF, ventral fascicle. Scale bars: 100 μm (A–L).
All spinigers with long blades finely serrated (Fig.
A–E Nereis tricirrata sp. nov. holotype (TIO-BTS-Poly-137) and F paratype (TIO-BTS-Poly-138) A notochaetae, homogomph spiniger, chaetiger 40 B neurochaetae, homogomph spiniger, dorsal fascicle, chaetiger 5 C neurochaetae, heterogomph spiniger, ventral fascicle, chaetiger 40 D notochaetae, homogomph falciger, chaetiger 40 E neurochaetae, heterogomph falciger, dorsal fascicle, chaetiger 20 F notochaetae, homogomph falciger, posterior parapodia. Scale bars: 50 μm (A–F).
Posterior end with six or seven regenerated chaetigers (Fig.
The specific epithet tricirrata is composed by the Latin prefix tri-, meaning three, and the Latin noun cirrus, and refers to the three anal cirri present on the pygidium, one on the mid-dorsal and one on each of the ventro-lateral sides.
Currently only known from the deep-sea sedimentary habitat in the northern South China Sea.
Deep-sea soft sediments characterized by foraminiferal ooze at depths between 1100 m and 1800 m.
There are no identical sequence matches on GenBank for COI and 16S. The low 18S gene divergence (0–1.9% K2P) between Nereis tricirrata sp. nov. and other Nereis species revealed their close genetic relationship, including an eyeless species, Nereis sanderi Blake, 1985 (AM159579). The reconstructed phylogenetic tree (Fig.
The mtCOI-based genetic divergence (K2P) between described Nereis species with the available sequences.
Taxa | Locality | 1 | 2 | 3 | 4 | 5 | 6 | 7 | 8 | 9 | 10 | 11 | |
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1 | N. multignatha MT712473 | China | |||||||||||
2 | N. pelagica HQ023592 | Canada | 0.286 | ||||||||||
3 | N. vexillosa HM473512 | Canada | 0.285 | 0.259 | |||||||||
4 | N. zonata HQ024404 | Canada | 0.262 | 0.238 | 0.284 | ||||||||
5 | N. denhamensis JX294511 | Australia | 0.313 | 0.336 | 0.302 | 0.335 | |||||||
6 | N. falsa KR916890 | Portugal | 0.344 | 0.282 | 0.330 | 0.339 | 0.360 | ||||||
7 | N. heterocirrata MN256589 | China | 0.291 | 0.263 | 0.304 | 0.317 | 0.309 | 0.343 | |||||
8 | N. eakini MN138408 | USA | 0.238 | 0.242 | 0.250 | 0.272 | 0.343 | 0.338 | 0.314 | ||||
9 | N. riisei JF293304 | Colombia | 0.304 | 0.294 | 0.312 | 0.262 | 0.351 | 0.313 | 0.291 | 0.324 | |||
10 | N. heronensis JX392066 | Australia | 0.287 | 0.248 | 0.311 | 0.306 | 0.332 | 0.364 | 0.302 | 0.319 | 0.336 | ||
11 | N. lizardensis JX392060 | Australia | 0.290 | 0.307 | 0.296 | 0.306 | 0.277 | 0.320 | 0.291 | 0.287 | 0.303 | 0.327 | |
12 | N. tricirrata sp. nov. OP292645 | SCS | 0.288 | 0.231 | 0.254 | 0.275 | 0.337 | 0.359 | 0.308 | 0.267 | 0.373 | 0.344 | 0.314 |
The maximum likelihood (ML) tree inferred from the concatenated sequences of three genes (mtCOI, 16S and 18S rRNA) with GenBank accession numbers. Bootstrap values and posterior probabilities values at nodes were calculated from the ML and Bayesian inference (BI) analyses, respectively. Only bootstrap values ≥ 50 and posterior probabilities ≥ 0.7 are shown. GenBank accession numbers in parenthesis are present in the order of COI, 16S, and 18S; missing markers are denoted by a dash (–).
Nereis tricirrata sp. nov. is distinguished from most Nereis species around the world by the absence of eyes on the prostomium. With the new species in this study, seven other described Nereis species from the deep Pacific also lack prostomial eyes. Six of these species belong to a distinct group with greatly prolonged notopodia in the posterior parapodia, including N. profundi Kirkegaard, 1956, N. anoculis Hartman, 1960, N. anoculopsis Fauchald, 1972, N. sandersi Blake, 1985, N. piscesae Blake & Hilbig, 1990, and N. abyssa Imajima, 1990. Comparison of the two eyeless species bearing normal notopodia throughout the body showed that Nereis tricirrata sp. nov. differs from Nereis izukai Okuda, 1939 (
We are grateful to the captain and crew of the R/V ‘Haiyangdizhi 10’ for help in collecting the deep-sea samples during the cruise organized by the Guangzhou Marine Geological Survey (Guangzhou, China). We thank Drs Chris Glasby and Torkild Bakken for their valuable comments that improved the manuscript. This study was supported by the National Natural Science Foundation of China (42006127), the Marine Geological Survey Program of China Geological Survey (DD20221706), and the Scientific Research Foundation of Third Institute of Oceanography, MNR (2016043).
DNA sequences with GenBank accession numbers used for the phylogenetic analysis; new sequences in bold.
Species | Localities | Voucher/isolate | CO1 | 16S | 18S | References |
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Alitta succinea | USA | USNM: lZ: 1286800 | KT959389 | KT959483 | AY210447* | 18S from |
Alitta virens | UK (COI, 16S); France (18S) | – | OW028587 | OW028587 | Z83754* | 18S from |
Ceratocephale abyssorum | Abyssal SE Atlantic | – | GQ426683 | GQ426618 | GQ426585 |
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Ceratocephale loveni | Sweden | SMNH 83517 | – | DQ442614 | DQ442616 |
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Dendronereis aestuarina | India | – | KT964060 | – | KT900288 | Direct submission |
Hediste atoka | Japan | – | LC323003 | LC323039 | LC323073 |
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Hediste diadroma | Japan | – | LC323012 | LC323062 | LC323646 |
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Hediste diversicolor | Japan | – | LC323076 | LC323093 | LC381864 |
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Hediste japonica | Japan | – | LC323024 | LC323064 | LC323647 |
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Laeonereis culveri | Brazil | – | MH264893 | MH264663 | MW826082 | Direct submission |
Namalycastis hawaiiensis | Narashino, Japan | isolate 35–1 | LC213726 | LC213728 | LC213729 |
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Namalycastis jaya | Kerala, India | AQJ3 | JN790066 | JX483869 | JX483866 |
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Neanthes acuminata | California, USA | isolate RLF3 | KJ539109 | KJ538992 | – |
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Neanthes glandicincta | Xiamen, China | 497 | KY094478 | KY094478 | – |
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Nereis heterocirrata | China | – | KC800626 | KC833492 | KC840694 | Direct submission |
Nereis pelagica | Sweden | SMNH118992; SMNH 75831 | JN852947 | AY340470 | AY340438 |
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Nereis tricirrata sp. nov. | deep SCS | TIO–BTS–Poly–137 | OP292645 | OP292646 | OP292647 | This study |
Nereis vexillosa | Alaska (COI); China (16S); Germany (18S) | – | MF121002 | GU362677 | DQ790083 | Direct submission |
Perinereis aibuhitensis | China | – | KC800612 | KC833486 | KC840692 | Direct submission |
Perinereis brevicirris | China | – | KC800630 | KC833498 | – | Direct submission |
Perinereis cultrifera | China | – | KC800624 | KC833495 | – | Direct submission |
Perinereis nuntia | Korea | – | JX644015 | JX644015 | – |
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Perinereis wilsoni | China | – | KC800631 | KC833497 | KC840691 | Direct submission |
Platynereis dumerilii | USA (COI & 16S); UK (18S) | – | AF178678 | AF178678 | EF117897 | COI & 16S from |
Pseudonereis variegata | China | – | KC800622 | KC833493 | KC840693 | Direct submission |
Gyptis pacifica | Japan | SIO–BIC A2516, A2517 | JN631314 | JN631322 | JN631337 |
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Gyptis brunnea | California, USA | FP collection | JN631313 | JN631323 | JN631335 |
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