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Research Article
Podarkeopsis chinensis sp. nov. (Annelida, Hesionidae) from southeastern China
expand article infoShan Tong‡§, Deyuan Yang|‡, Jian-Wen Qiu#, Caihuan Ke‡, Zhi Wang‡
‡ Xiamen University, Xiamen, China
§ Zhejiang Ocean University, Zhoushan, China
| National Taiwan Ocean University, Keelung, Taiwan
¶ Hong Kong Baptist University, Hong Kong, Hong Kong
# Southern Marine Science and Engineering Guangdong Laboratory, Guangzhou, China

Corresponding author: Zhi Wang ( zhiwang00kxy@xmu.edu.cn )

Academic editor: Christopher Glasby
© 2023 Shan Tong, Deyuan Yang, Jian-Wen Qiu, Caihuan Ke, Zhi Wang.
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: Tong S, Yang D, Qiu J-W, Ke C, Wang Z (2023) Podarkeopsis chinensis sp. nov. (Annelida, Hesionidae) from southeastern China. ZooKeys 1173: 339-355. https://doi.org/10.3897/zookeys.1173.106112
ZooBank: urn:lsid:zoobank.org:pub:4F949981-76B5-4758-8D41-012D55D46529
Open Access

Abstract

Podarkeopsis chinensis sp. nov. (Annelida, Hesionidae) is described based on specimens collected from the coast of southeast China. It is the first Podarkeopsis species described from the Indo-Pacific, although there are already nine valid Podarkeopsis species known from other parts of the world. This new species can be distinguished from the other Podarkeopsis species in having a palpostyle as long as the palpophore and double aciculae in both notopodia and neuropodia, and in bearing bifid furcate chaetae which have a smooth base on the shorter tine. A phylogenetic analysis based on the concatenated sequences of five gene fragments (COI, 16S rRNA, 18S rRNA, 28S rRNA, and histone H3) from 18 specimens of P. chinensis sp. nov. showed that they formed a monophyletic clade that is sister to P. levifuscina. K2P genetic distances indicated that the four gene fragments (COI, 16S rRNA, 18S rRNA, and 28S rRNA) of P. chinensis sp. nov. diverged from the corresponding sequences of the closest related species of Podarkeopsis in GenBank and BOLD Systems by 21.1–27.5%, 20.3–23.1%, 0.1–0.2%, and 2.1–3.2%. An identification key is provided for species in the genus Podarkeopsis.

Key words

Identification key, Indo-Pacific, molecular phylogeny, morphology, new species, polychaete, systematics

Introduction

Podarkeopsis Laubier, 1961 is a genus of small-bodied polychaetes in the family Hesionidae and currently comprises nine species (Read and Fauchald 2023), including three species from Europe, two species from the Pacific coast of the United States, one species from the Atlantic coast of the United States, one species from the Pacific coast of Central America, one species from the Atlantic coast of Central America, and one species from the Atlantic coast of South Africa (Fig. 1). Although Podarkeopsis species have unique morphological characteristics including having 10 triangular papillae, a pair of palps and three antennae placed towards the anterior prostomial margin, and eight pairs of tentacular cirri, its species diversity and phylogenetic relationships remain poorly understood, partially due to their minute size (a complete specimen is 5–18 mm long, 1–2 mm wide, and with 25–46 chaetigers), making them difficult to collect.

Figure 1. 

Type localities of Podarkeopsis species around the world (red spots and numbers, data from Read and Fauchald 2023) and records of Podarkeopsis from the China seas (blue triangles and letters). Numbers next to the red circles represent 1 P. arenicolus (La Greca, 1946), Gulf of Naples 2 P. brevipalpa (Hartmann-Schröder, 1959), El Salvador EEZ 3 P. galangaui Laubier, 1961, Banyuls, France 4 P. glabrus (Hartman, 1961), Southern California 5 P. capensis (Day, 1963), South Africa 6 P. helgolandicus (Hilbig & Dittmer, 1979), Helgoland, Germany 7 P. levifuscina Perkins, 1984, North Carolina, USA 8 P. guadalupensis Amoureux, 1985, Caribbean Costa Rica 9 P. perkinsi Hilbig, 1992, California, US 10 P. chinensis sp. nov., Daya Bay, Guangdong, China (this study). Letters corresponding to the blue triangles along southeastern China represent a P. sp. A & B, Hong Kong (Shin 1998) b P. sp., Beibu Gulf (Wang 2008) c P. galangani, Daya Bay, Guangdong (Li 2010) d P. sp., Daya Bay, Guangdong (Du et al. 2011) e P. sp., Hong Kong (Wang et al. 2017) f P. sp., Daya Bay, Guangdong (Zhang 2017) g P. chinensis sp. nov., Daya Bay, Guangdong and ZhaoAn Bay, Fujian (this study). Source of map: No. GS(2016)1563.

Currently, there are only a few studies with a description or specimen records of Podarkeopsis from Indo-Pacific. Imajima (2007) described P. brevipalpa (Hartmann-Schröder, 1959) and P. glabrus (Hartman, 1961) based on specimens collected from Japanese waters, which is the only morphological record of Podarkeopsis in the Indo-Pacific. However, this record is questionable, as the type locality of P. brevipalpa is the coast of El Salvador in Central America, and the type locality of P. glabrus is in southern California (Fig. 1). In addition, Podarkeopsis, mostly identified to the genus level, has been recorded in several ecological studies in the China seas (Shin 1998; Wang 2008; Li 2010; Du et al. 2011; Wang et al. 2017; Zhang 2017). Podarkeopsis galangani (a misspelling of P. galangaui Laubier, 1961) has been reported from Daya Bay, Guangdong, China, but this record is questionable, given that its type locality is the Mediterranean coast of France (Li 2010).

In this study, we describe and illustrate a new species, Podarkeopsis chinensis sp. nov., based on specimens collected from Daya Bay, Guangdong and ZhaoAn Bay, Fujian in southern China. We sequenced five gene fragments (COI, 16S rRNA, 18S rRNA, 28S rRNA, and histone H3) to determine the phylogenetic position of the new species within Podarkeopsis.

Material and methods

Sample collection and preservation

Eighteen specimens (holotype: XMU-Pol-2021-105, paratype 1: XMU-Pol-2021-106, paratype 2 MBM287621, paratype 3: XMU-Pol-2021-197, paratype 4: XMU-Pol-2021-201, paratype 5: XMU-Pol-2021-203, paratype 6: XMU-Pol-2021-204, paratype 7: XMU-Pol-2021-205, paratype 8: XMU-Pol-2021-207, paratype 9: XMU-Pol-2021-208, paratype 10: XMU-Pol-2021-209, paratype 11: XMU-Pol-2021-213, paratype 12: XMU-Pol-2021-214, paratype 13: XMU-Pol-2021-215, paratype 14: MBM287622, paratype 15: XMU-Pol-2021-221, paratype 16: XMU-Pol-2021-223, paratype 17: XMU-Pol-2021-224) were collected from the coastal waters of southeast China in 2021 (see Materials examined for details). Sediments were sorted with a 0.5 mm sieve, and the retained materials including the specimens were anaesthetized with 7% MgCl2 solution, transferred to 50% ethanol for preliminary fixation, and then to 100% ethanol for final fixation. Podarkeopsis specimens were picked out under a stereomicroscope M165C in the laboratory, preliminarily identified to species, and preserved for further morphological and molecular analyses. Two specimens of P. chinensis sp. nov. (paratype 2, paratype 14) were deposited in the Marine Biological Museum, Chinese Academy of Sciences (MBMCAS), and the other 16 specimens of P. chinensis sp. nov. (holotype, paratypes 1, paratypes 3–13, and paratypes 15–17) were deposited in the specimen collections of the College of Ocean and Earth Sciences, Xiamen University (XMU).

Morphological analysis

Selected parapodia of the holotype (XMU-Pol-2021-105), paratype 10 (XMU-Pol-2021-209) and paratype 12 (XMU-Pol-2021-214) were dissected with iridectomy scissors and permanently mounted on slides for observation of their gross morphology and chaetae, as well as for photography. To observe the minute teeth inside the pharynx, the anterior region of the paratype 6 (XMU-Pol-2021-204), paratype 11 (XMU-Pol-2021-213), and paratype 13 (XMU-Pol-2021-215) were hyalinized with graded series of glycerol (30%, 60%, 100%), mounted on slides and compressed slowly with a cover glass. Photographs of the whole specimen and parapodia (with chaetae) were taken using a camera DMC5400 mounted on a Leica M165C stereomicroscope. Photographs were taken at different focuses and stacked into fully focused images using Helicon Focus v. 7 as described by Wang et al. (2018). The anterior region of the paratype 5 (XMU-Pol-2021-203) and paratype 12 (XMU-Pol-2021-214) were treated by critical point drying and fixed on a conductive adhesive for gold plating. Photographs of the anterior end were taken using Phenom ProX scanning electron microscope (SEM). The classification of the type of parapodia following Jarvis (2011): biramous with many emergent notochaetae; sub-biramous with few emergent notochaetae; sesquiramous with acicula inside cirrophore and without emergent chaetae.

DNA extraction, PCR amplification, and sequencing

Eighteen specimens of Podarkeopsis chinensis sp. nov. were used for DNA extraction. For each specimen, a few segments were dissected, and genomic DNA was extracted with a DNeasy Blood & Tissue Kit (QIAGEN). Five primer pairs were used to amplify corresponding gene fragments, viz., PolyLCO and PolyHCO for the mitochondrial COI gene fragment (Carr et al. 2011), 16SAR-L and 16SBR-H for the mitochondrial 16S rRNA gene fragment (Palumbi et al. 1991), 1F and 9R for the nuclear 18S rRNA gene fragment (Glover et al. 2016); NLF184/21 and D3aR for the nuclear 28S rRNA gene fragment (Lenaers et al. 1989; Van der Auwera et al. 1994) and H3af and H3ar for the Histone H3 gene fragment (Colgan et al. 1998). The PCR protocol followed Zhang et al. (2018). The PCR products were checked by electrophoresis in a 2% agarose gel, and sequenced using Sanger sequencing at Xiamen Borui Biological Technology Co., Ltd.

Phylogenetic analyses

The sequences of the five gene fragments generated in this study, together with those of all corresponding Podarkeopsis and two Oxydromus species (outgroup) available in GenBank (https://www.ncbi.nlm.nih.gov/Genbank) and BOLD (http://www.barcodinglife.org), were used for phylogenetic analyses (Table 1). The five gene sequences were aligned using the MUSCLE algorithm (Edgar 2004). The poorly aligned positions were removed with the Gblocks v. 0.91b plugged in PhyloSuite v. 1.2.3 (Zhang et al. 2020). Phylogenetic analyses were conducted using the maximum-likelihood (ML, IQ-TREE v.2.2.0 plugged in PhyloSuite) and Bayesian-inference (BI, MrBayes v.3.2.7a plugged in PhyloSuite) methods. Specifically, the ML analysis with IQ-TREE (Nguyen et al. 2015) was conducted using the “ultrafast bootstrap” option with a bootstrap number of 10,000. The best-fit evolutionary model GTR+I+G was selected for the BI analysis using ModelFinder v. 2.2.0 based on the Bayesian Information Criterion (BIC) (Kalyaanamoorthy et al. 2017). The BI analysis was conducted using MrBayes with Markov Chains run for 10,000,000 generations and topologies sampled every 1000 generations (Ronquist and Huelsenbeck 2003). The first 25% of trees were discarded as “burn-in” and the software Tracer v. 1.7.1 was used to check for the convergence of the trees (Rambaut et al. 2018). The resulting ML and BI trees were visualized using Figtree v. 1.4.4 (http://tree.bio.ed.ac.uk/software/figtree).

Table 1.
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Sequence accession numbers (GenBank and BOLD) and specimen information of Podarkeopsis and Oxydromus used in this study.

Taxon Origin Voucher/Sample ID COI 16S rRNA 18S rRNA 28S rRNA histone H3 Reference
Oxydromus obscurus North Carolina, USA GNM 86189 KJ855073 KJ855068 – KJ855080 – Martin et al. 2015
Oxydromus microantennatus Australia GNM 86192 KJ855072 KJ855067 – KJ855079 – Martin et al. 2015
Podarkeopsis arenicolus France SMNH 83509 JN571827 JN571879 JN571889 DQ442609 – Ruta et al. 2007; Summers et al. 2015
Podarkeopsis capensis Saudi Arabia Itsastk13-P113 KT307681 – – – – Aylagas et al. 2016
*Podarkeopsis glabrus Washington, USA 2849_DNA BBPS549-19 – – – – BOLD direct submission
*Podarkeopsis glabrus Washington, USA 2852_DNA BBPS550-19 – – – – BOLD direct submission
*Podarkeopsis glabrus Washington, USA 2854_DNA BBPS551-19 – – – – BOLD direct submission
*Podarkeopsis glabrus Washington, USA 2857_DNA BBPS552-19 – – – – BOLD direct submission
*Podarkeopsis glabrus Washington, USA 2863_DNA BBPS553-19 – – – – BOLD direct submission
*Podarkeopsis glabrus California, USA MBI-SCCWRP-00412 CMBIA476-11 – – – – BOLD direct submission
Podarkeopsis helgolandicus Sweden SE07DNA4 JN631311 – JN631331 JN631344 – Pleijel et al. 2012
Podarkeopsis levifuscina Florida, USA SERCINVERT2330 OQ323143 – – – – Genbank direct submission
Podarkeopsis perkinsi California, USA SIO-BIC A2339 JN571828 JN571881 JN571892 JN571901 – Summers et al. 2015
*Podarkeopsis sp. (as Oxydromus angustifrons) Laizhou Bay, Shandong, China BIOUG03550-B01 HZPLY108-12 – – – – BOLD direct submission
*Podarkeopsis sp. (as Oxydromus angustifrons) Northern Yellow Sea,China BIOUG06836-E09 HZPLY627-13 – – – – BOLD direct submission
*Podarkeopsis sp. (as Oxydromus angustifrons) Laizhou Bay, China BIOUG06836-E11 HZPLY629-13 – – – – BOLD direct submission
Podarkeopsis chinensis sp. nov. Daya Bay, Guangdong, China XMU-Pol-2021-105 MZ322693 MZ330781 OK044387 MZ344143 MZ272434 This study
Podarkeopsis chinensis sp. nov. Daya Bay, Guangdong, China XMU-Pol-2021-106 MZ322694 MZ330782 OK044388 – MZ272435 This study
Podarkeopsis chinensis sp. nov. Daya Bay, Guangdong, China MBM287621 MZ873348 MZ890235 OK044406 MZ870391 MZ695068 This study
Podarkeopsis chinensis sp. nov. Daya Bay, Guangdong, China XMU-Pol-2021-197 MZ873349 MZ890238 OK044409 MZ870394 MZ695069 This study
Podarkeopsis chinensis sp. nov. ZhaoAn Bay, Fujian, China XMU-Pol-2021-201 MZ820673 MZ890241 OK044410 MZ820369 MZ889051 This study
Podarkeopsis chinensis sp. nov. ZhaoAn Bay, Fujian, China XMU-Pol-2021-203 MZ820674 MZ890243 OK044412 MZ820371 MZ889053 This study
Podarkeopsis chinensis sp. nov. ZhaoAn Bay, Fujian, China XMU-Pol-2021-204 MZ820675 MZ890244 OK044413 MZ820372 MZ889054 This study
Podarkeopsis chinensis sp. nov. ZhaoAn Bay, Fujian, China XMU-Pol-2021-205 MZ820676 MZ890245 OK044414 MZ820373 MZ889055 This study
Podarkeopsis chinensis sp. nov. ZhaoAn Bay, Fujian, China XMU-Pol-2021-207 MZ820677 MZ890247 OK044415 MZ820375 MZ889057 This study
Podarkeopsis chinensis sp. nov. ZhaoAn Bay, Fujian, China XMU-Pol-2021-208 MZ820678 MZ890248 OK044416 MZ820376 MZ889058 This study
Podarkeopsis chinensis sp. nov. ZhaoAn Bay, Fujian, China XMU-Pol-2021-209 MZ820679 MZ890249 MZ870412 MZ820377 MZ889059 This study
Podarkeopsis chinensis sp. nov. ZhaoAn Bay, Fujian, China XMU-Pol-2021-213 MZ820680 MZ890253 OK044419 MZ820381 MZ889063 This study
Podarkeopsis chinensis sp. nov. ZhaoAn Bay, Fujian, China XMU-Pol-2021-214 MZ820681 MZ890254 OK044420 MZ820382 MZ889064 This study
Podarkeopsis chinensis sp. nov. ZhaoAn Bay, Fujian, China XMU-Pol-2021-215 MZ820682 MZ890255 OK044421 MZ870397 MZ889065 This study
Podarkeopsis chinensis sp. nov. ZhaoAn Bay, Fujian, China MBM287622 MZ820683 MZ890256 OK044422 MZ820383 MZ889066 This study
Podarkeopsis chinensis sp. nov. ZhaoAn Bay, Fujian, China XMU-Pol-2021-221 MZ873355 MZ890261 MZ870417 MZ870398 MZ889071 This study
Podarkeopsis chinensis sp. nov. ZhaoAn Bay, Fujian, China XMU-Pol-2021-223 MZ873357 MZ890263 OK044426 MZ870400 MZ889073 This study
Podarkeopsis chinensis sp. nov. ZhaoAn Bay, Fujian, China XMU-Pol-2021-224 MZ873358 MZ890264 OK044427 MZ870401 MZ889074 This study

Note: *, data from BOLD Systems; the other data were from GenBank. –, Data not available.

K2P genetic distances

K2P genetic distances represent the standard in DNA barcoding literature and therefore facilitate comparisons (Čandek and Kuntner 2015). Intraspecific and interspecific K2P genetic distances of the five aligned gene sequences of Podarkeopsis species were calculated based on each gene sequence using Kimura 2-parameter (K2P) (Kimura 1980) in MEGA X. The ratio of transitions and tranversions at the first, second, and third codon positions in pairwise comparisons of aligned data set was plotted against the sequence difference values for five gene fragments (Kumar et al. 2018).

Results

Systematics

Family Hesionidae Grube, 1850

Subfamily Ophiodrominae Pleijel, 1998

Tribe Ophiodromini Pleijel, 1998

Podarkeopsis Laubier, 1961

Type species

Podarkeopsis galangaui Laubier, 1961.

Type locality

Banyuls, France.

Podarkeopsis chinensis sp. nov.

https://zoobank.org/E34C0784-0B1E-4EE7-AF72-06F612CC5BCA
Figs 1, 2, 3, 4, 5, Table 1, 2

Materials examined

Holotype : China; Guangdong, Daya Bay, Guishan Island; 22°49'4"N, 114°47'11"E; 1 April 2021; Deyuan Yang, Zhi Wang leg.; intertidal zone; XMU-Pol-2021-105, the anterior fragment with 21 chaetigers, length: 3.4 mm, width without parapodia: 0.6 mm. Paratypes: China; Guangdong, Daya Bay, Guishan Island; 22°49'4"N, 114°47'11"E; 1 April 2021; Deyuan Yang, Zhi Wang leg.; intertidal zone; paratype 1 (XMU-Pol-2021-106), the anterior fragment with 16 chaetigers, length: 3.4 mm, width without parapodia: 0.6 mm. China; Guangdong, Daya Bay; 22°41'2"N, 114°37'17"E/5.6 m; 13 March 2021; Zhi Wang, Lizhe Cai, Kang Mei, Xiaoyu Zhao leg.; shallow subtidal muddy sediment; paratype 2 (MBM287621), the anterior fragment with 15 chaetigers, length: 3.0 mm, width without parapodia: 0.6 mm; paratype 3 (XMU-Pol-2021-197), the anterior fragment with 13 chaetigers, length: 2.0 mm, width without parapodia: 0.6 mm. CHINA; Fujian, ZhaoAn Bay; 23°43'14"N, 117°17'22"E/2.6 m depth; 28 May 2021; Zhi Wang, Yuyao Li leg.; shallow subtidal hard muddy sediment; paratype 4 (XMU-Pol-2021-201), the anterior fragment with 11 chaetigers, length: 1.7 mm, width without parapodia: 0.6 mm; paratype 5 (XMU-Pol-2021-203), the anterior fragment with 10 chaetigers, length: 1.4 mm, width without parapodia: 0.6 mm; paratype 6 (XMU-Pol-2021-204), the anterior fragment with 14 chaetigers, length: 2.8 mm, width without parapodia: 0.7 mm. China; Fujian, ZhaoAn Bay; 23°42'30"N, 117°18'36"E/2.6 m depth; 28 May 2021; Zhi Wang, Yuyao Li leg.; shallow subtidal hard muddy sediment; paratype 7 (XMU-Pol-2021-205), the anterior fragment with 15 chaetigers, length: 3.2 mm, width without parapodia: 0.6 mm; paratype 8 (XMU-Pol-2021-207), the anterior fragment with 14 chaetigers, length: 2.9 mm, width without parapodia: 0.6 mm; paratype 9 (XMU-Pol-2021-208), the anterior fragment with 14 chaetigers, length: 2.1 mm, width without parapodia: 0.7 mm; paratype 10 (XMU-Pol-2021-209), the anterior fragment with 16 chaetigers, length: 3.0 mm, width without parapodia: 0.6 mm. China; Fujian, ZhaoAn Bay; 23°43'11"N, 117°18'11"E/3.5 m depth; 28 May 2021; Zhi Wang, Yuyao Li leg.; shallow subtidal hard muddy sediment; paratype 11 (XMU-Pol-2021-213), the anterior fragment with 21 chaetigers, length: 3.5 mm, width without parapodia: 0.6 mm; paratype 12 (XMU-Pol-2021-214), the anterior fragment with 21 chaetigers, length: 3.9 mm, width without parapodia: 0.6 mm; paratype 13 (XMU-Pol-2021-215), the anterior fragment with 14 chaetigers, length: 3.1 mm, width without parapodia: 0.7 mm; paratype 14 (MBM287622), the anterior fragment with 2 chaetigers, length: 0.9 mm, width without parapodia: 0.5 mm. China; Fujian, ZhaoAn Bay; 23°42'34"N, 117°20'12"E/2.4 m depth; 28 May 2021; Zhi Wang, Yuyao Li leg.; shallow subtidal hard muddy sediment; paratype 15 (XMU-Pol-2021-221), the anterior fragment with 10 chaetigers, length: 1.5 mm, width without parapodia: 0.6 mm; paratype 16 (XMU-Pol-2021-223), the anterior fragment with 9 chaetigers, length: 1.4 mm, width without parapodia: 0.6 mm; paratype 17 (XMU-Pol-2021-224), the anterior fragment with 10 chaetigers, length: 1.5 mm, width without parapodia: 0.6 mm.

Diagnosis

Two pairs of eyes arranged in a trapezoid shape. Palps one pair, biarticulated, palpostyle as long as the palpophore. Double aciculae in both notopodia and neuropodia. Notopodial furcate chaetae present, base of the shorter tine smooth.

Description

(based on holotype, unless otherwise stated). Anterior fragment with 1–21 chaetigers. Body cylindrical. Fixed specimens uniformly pale (Fig. 2A, B).

Figure 2. 

Morphology of Podarkeopsis chinensis sp. nov. A, B, I holotype (XMU-Pol-2021-105) C–G, M paratype 5 (XMU-Pol-2021-203) J paratype 6 (XMU-Pol-2021-204) K paratype 11 (XMU-Pol-2021-213) L paratype 13 (XMU-Pol-2021-215) H, N paratype 12 (XMU-Pol-2021-214) A, B whole worm, dorsal and ventral view C, D anterior end, dorsal view, a dashed rectangular frame in D showing the position of nuchal organs E, F nuchal organs encircled by a dashed line G ring of papillae at the anterior edge of pharynx, inset: an papilla in detail H, I minute teeth on the inner wall of pharynx (white arrows), anterior view J–L minute teeth observed through pressed pharynx wall, dorsal view, inset in J showing enlarged minute tooth M tentacular cirri with most cirrostyles missing, right side, anterior view N chaetiger 1–3, right side, anterior view. Abbreviations: pr, prostomium; mAn, middle antenna; lAn, lateral antenna; pa, palp; no, nuchal organs; pap, papillae; tc, tentacular cirrus; dc, dorsal cirrus; vc, ventral cirrus; cs, cirrostyle; cp, cirrophore. Scale bars: 500 μm (A, B); 200 μm (C, D, G, J–L); 100 μm (E, F, H); 20 μm (insets in G and J).

Prostomium twice as wide as long. Eyes two pairs, placed towards the posterior prostomial margin, trapezoidally arranged, anterior pair kidney-shaped, larger than posterior pair, posterior pair oval (Fig. 2A, B). Palps one pair, biarticulated, palpostyle as long as palpophore. Three antennae, tapered. Median antenna thinner than lateral ones, lost in holotype, about half the length of lateral ones in paratype 5 (Fig. 2A, C, D). Nuchal organs of paratype 5 on lateral-posterior edge of prostomium (Fig. 2E, F). Pharynx strong, reversible, anterior edge with 10 triangular papillae (Fig. 2A, B, G). Teeth, minute, one pair, nearly triangular, symmetrically distributed on the inner wall of pharynx, visible from anterior view of pharynx in both holotype and paratypes (Fig. 2H–L). Tentacular cirri eight pairs, biarticulated, most cirrostyles missing (Fig. 2A, B).

Parapodia sesquiramous with acicula in cirrophore and without protruding notopodial chaetae in chaetigers 1–3 (Fig. 3A–C), biramous thereafter (Fig. 3D–I). Notopodial aciculae one pair, extending into cirrophores in chaetigers 1–4, extending into a small notopodial lobe in following chaetigers (Fig. 3A–I). Notopodial cirri digitate, about twice the length of neuropodial lobe, neuropodial cirri thinner, not longer than neuropodial lobe (Fig. 3C, E–G, J). Neuropodial aciculae one pair, neuropodial lobe in anterior chaetigers developed, prechaetal lobe long, digitated, postchaetal lobe rounded (Fig. 3A–F).

Figure 3. 

Parapodia of Podarkeopsis chinensis sp. nov. A–I parapodia of holotype (XMU-Pol-2021-105) J, K parapodia of paratype 10 (XMU-Pol-2021-209) L parapodia of paratype 12 (XMU-Pol-2021-214). A chaetiger 1, right side, posterior view B chaetiger 2, right side, anterior view C–E chaetiger 3–5, right side, posterior view F chaetiger 12, right side, anterior view G chaetiger 13, left side, posterior view H chaetiger 19, left side, anterior view I chaetiger 20, right side, anterior view. J chaetiger 3, left side, posterior view K chaetiger 13, left side, anterior view L chaetiger 13, right side, posterior view. Insets in A–E show numbers of notopodial and neuropodial aciculae. Insets in F show a small notopodial lobe with five notochaetae. Scale bars: 100 μm (A–L); 10 μm (insets in A–F).

Notochaetae 3 types. Furcate chaetae 2 or 3, bifid, base of the shorter tine smooth, longer tine about 2.3 times as long as shorter one (Fig. 4A–D). Acicular chaetae blunt, 1 or 2 (Fig. 4A, C, D). Capillary chaetae smooth and slender, longer than furcate chaetae and acicular chaetae, 1 or 2 in number (Fig. 4A, C, D). Neurochaetae all composite falcigers (Fig. 4E–H). Blade of all falcigers unidentate, blade length/width ratios ranging from 7 to 80 (Fig. 4F–H). Hooded neurochaetae rarely present, 0 or 1 per parapodia; if present, in subacicular bundle of neurochaetae (Fig. 4F2, H2).

Figure 4. 

Chaetae of Podarkeopsis chinensis sp. nov. A, C, D, F–H holotype (XMU-Pol-2021-105), light microscope; B, E paratype 5 (XMU-Pol-2021-203), scanning electron microscope. A–D notochaetae A1 forked chaeta A2 acicular chaeta A3 capillary chaeta, chaetiger 5 B furcate chaetae, chaetiger 5 C1 forked chaetae C2 acicular chaeta C3, C4 capillary chaetae, chaetiger 11 D1 forked chaetae D2, D3 acicular chaetae D4 capillary chaeta, chaetiger 19 E–H neuropodial falcigers E, F chaetiger 1 G chaetiger 11 H chaetiger 19. Scale bars: 200 μm (A, C, D, F3–F5, G2–G4, H3–H5); 10 μm (B); 15 μm (E); 300 μm (F1, F2, G1, H1, H2).

Intraspecific variation

Examination of the holotype and several paratypes of P. chinensis sp. nov. revealed different numbers of the three kinds of notochaetae. In the holotype, there were 2 or 3 furcate chaetae, 1 or 2 acicular chaetae, and 1 or 2 capillary chaetae. However, several paratypes had 2–4 furcate chaetae, 1–4 acicular chaetae, and 1–3 capillary chaetae. The number of these chaetae may be related to the developmental stages or environmental conditions.

Remarks

The new species can be distinguished from the other nine species of the genus in having 1) median antenna about half as long as lateral ones, while P. arenicolus, P. brevipalpa, P. galangaui, P. glabrus, and P. helgolandicus have median antenna shorter than half of the lateral ones (Hartmann-Schröder 1959; Hartman 1961; Laubier 1961; Hilbig and Dittmer 1979; Rizzo and Salazar-Vallejo 2014); another species, P. perkinsi, however, has median antenna about two-thirds as long as lateral one (Hilbig 1992); 2) ventral cirri as long as, or barely shorter than neuropodial lobe, while P. brevipalpa, P. galangaui, and P. glabrus have ventral cirri apparently longer than neuropodial lobe (Hartmann-Schröder 1959; Hartman 1961; Laubier 1961), P. guadalupensis and P. levifuscina have ventral cirri markedly shorter than neuropodial lobe (Amoureux 1985; Perkins 1984); 3) double aciculae in both notopodia and neuropodia, while P. capensis, P. glabrus, and P. perkinsi have one aciculae in both notopodia and neuropodia (Day 1963; Hartman 1961; Hilbig 1992), and P. levifuscina has one acicula in notopodia and double aciculae in neuropodia (Perkins 1984); and 4) notopodial furcate chaetae with both handles smooth, while P. galangaui, P. glabrus, P. guadalupensis, P. helgolandicus, and P. perkinsi have notopodial furcate chaetae with denticulated at the base of either the shorter handle or both handles (Hartman 1961; Laubier 1961; Hilbig and Dittmer 1979; Amoureux 1985; Hilbig 1992).

Etymology

The specific name chinensis is an adjective in the nominative singular, derived from China, where the specimens were collected. The suggested formal Chinese name for this species is “中国健足虫”.

Habitat

Intertidal, shallow subtidal muddy sediment.

Distribution

Podarkeopsis chinensis sp. nov. is currently known from Daya Bay, Guangdong and ZhaoAn Bay, Fujian, China. It is expected that this species is widely distributed along the coast of southeast China.

Phylogenetic analysis

The ML tree and BI tree, reconstructed based on the 3943-bp concatenated sequences, showed consistent topologies clustering the eight analyzed Podarkeopsis species within a single clade with high support values (BS = 100; BPP = 1) (Fig. 5). All 18 specimens of Podarkeopsis chinensis sp. nov. were clustered within a clade with high support values (BS= 100, BPP = 1), and P. chinensis sp. nov. was sister to P. levifuscina collected from Florida, USA (BS = 79; BPP = 0.84). The clade comprising the two species was sister to Podarkeopsis sp. (as Oxydromus angustifrons Grube, 1878) from Bohai Sea, China (BS = 86; BPP = 0.88). The results of phylogenetic analyses indicated P. chinensis sp. nov. could be distinguished as a new species by its clustering relationship with high support.

Figure 5. 

Phylogenetic trees of Podarkeopsis based on 3943-bp concatenated sequences of 636 bp COI, 496 bp 16S rRNA, 1554 bp 18S rRNA, 954 bp 28S rRNA and 304 bp histone H3 gene fragments A maximum-likelihood (ML) tree B Bayesian-inference (BI) tree. Vouchers (isolates) and accession numbers of the analyzed species are listed in Table 1. Branch support values refer to bootstrap (BS) and Bayesian posterior probabilities (BPP), and branch support values lower than 80 (BS) and 0.8 (BPP) are omitted. The scale bar indicates the number of substitutions per site.

K2P genetic distances

The average intraspecific K2P genetic distances of Podarkeopsis chinensis sp. nov. were 0.2% for COI and 16S rRNA gene fragments, 0.0% for 18S rRNA gene fragment, 0.1% for 28S rRNA gene fragment, and 0.5% for histone H3 gene fragment (Table 2). Besides, the interspecific genetic distances between P. chinensis sp. nov. and the other Podarkeopsis species ranged from 21.1–27.5% for COI gene fragment, 20.3–23.1% for 16S rRNA gene fragment, 0.1–0.2% for 18S rRNA gene, and 2.1–3.2% for 28S rRNA gene fragment.

Table 2.
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XLSX

Intraspecific and interspecific K2P genetic distances of the five gene fragments of all available Podarkeopsis species.

Species N Species
1 2 3 4 5 6 7 8
COI (585 bp)
1. Podarkeopsi arenicolus 1 –
2. Podarkeopsi capensis 1 0.005 –
3. Podarkeopsi glabrus 6 0.221 0.235 0.003
4. Podarkeopsi helgolandicus 1 0.227 0.224 0.265 –
5. Podarkeopsi levifuscina 1 0.232 0.230 0.250 0.240 –
6. Podarkeopsi perkinsi 1 0.227 0.223 0.233 0.237 0.227 –
7. Podarkeopsis sp. (as Oxydromus angustifrons) 3 0.218 0.223 0.258 0.227 0.225 0.250 0.009
8. Podarkeopsi chinensis sp. nov. 18 0.271 0.264 0.275 0.271 0.211 0.246 0.252 0.002
16S rRNA (389 bp)
1. Podarkeopsi arenicolus 1 –
2. Podarkeopsi perkinsi 1 0.192 –
3. Podarkeopsi chinensis sp. nov. 18 0.203 0.231 0.002
18S rRNA (854 bp)
1. Podarkeopsi arenicolus 1 –
2. Podarkeopsi helgolandicus 1 0.001 –
3. Podarkeopsi perkinsi 1 0.002 0.001 –
4. Podarkeopsi chinensis sp. nov. 18 0.002 0.001 0.002 0.000
28S rRNA (682 bp)
1. Podarkeopsi arenicolus 1 –
2. Podarkeopsi helgolandicus 1 0.019 –
3. Podarkeopsi perkinsi 1 0.032 0.028 –
4. Podarkeopsi chinensis sp. nov. 18 0.021 0.023 0.032 0.001
histone H3 (284 bp)
1. Podarkeopsi chinensis sp. nov. 18 0.005

Discussion

Although Podarkeopsis is a common genus of polychaete in intertidal and subtidal sediments, it has attracted little attention, possibly due to its small size, fragilility, and usually incomplete condition of fixed specimens. This genus can be clearly distinguished from other hesionid genera by several remarkable characteristics, such as having the pharynx with 10 papillae on the anterior edge (vs no papillae as in Oxydromus, Hesione, etc.; ~20 papillae as in Micropodarke) and bearing four pairs of tentacular cirri on both sides of the peristomium (vs three pairs as in Oxydromus, Micropodarke, Syllidia, etc.) (Pleijel 1998; Rizzo and Salazar-Vallejo 2014). Therefore, it is not difficult to identify specimens to the genus level.

The genus Podarkeopsis currently includes only nine valid species, and in this study we describe a tenth species, P. chinensis sp. nov., the first Podarkeopsis species described from the Indo-Pacific. Podarkeopsis cincinnata (Verrill, 1881) collected from New England, USA, has three pairs (instead of four as in other species of Podarkeopsis) of slender tentacular cirri on each side and about 12 papillae according to the original description; therefore, it is considered here an invalid species of Podarkeopsis, and its status could not be determined without checking the type material. In addition to P. chinensis sp. nov., we also found some other species of Podarkeopsis from the China seas, which indicated an underestimated species diversity of this genus. Given that many undescribed species of Podarkeopsis and several species in this region are potentially misidentified, we predict that further studies may lead to the discovery of more species.

In addition to the mentioned characteristics, we also noted two, minute teeth on the inner wall of the pharynx in all specimens of P. chinensis sp. nov. examined (Fig. 2H–L), but these teeth have not been reported from the other species of Podarkeopsis. Besides, we observed a special type of hooded neurochaetae that had not been reported from other species of Podarkeopsis, but a similar kind of chaeta had been noted from some other hesionid species (Perkins 1984: 579; Wang et al. 2018: fig. 3O, P; this study, Fig. 4F2, H2), Thus, further studies should explore the use of these additional characters to distinguish species in the genus.

Key to species of Podarkeopsis Laubier, 1961 (type locality given after species)

1 Median antenna shorter than half of the lateral ones 2
– Median antenna as long as, or longer than half of the lateral ones 5
2(1) Lateral antennae as long as palps P. glabrus (Hartman, 1961); California, USA
– Lateral antennae longer than palps 3
3(2) Palpophore as long as palpostyle P. galangaui Laubier, 1961; France
– Palpophore longer than palpostyle 4
4(3) Ventral cirri markedly longer than neuropodial lobe; notopodial furcate chaetae with handle smooth P. brevipalpa (Hartmann-Schröder, 1959); El Salvador
– Ventral cirri shorter than neuropodial lobe; notopodial furcate chaetae with handle denticulated P. helgolandicus (Hilbig & Dittmer, 1979); Helgoland, Germany
5(1) Median antenna about 2/3 as long as lateral one P. perkinsi Hilbig, 1992; California, USA
– Median antenna about half as long as lateral ones 6
6(5) Lateral antennae longer than palps P. arenicolus (La Greca, 1946); Gulf of Naples
– Lateral antennae as long as, or barely longer than palps 7
7(6) Ventral cirri markedly shorter than neuropodial lobe 8
– Ventral cirri as long as, or barely shorter than neuropodial lobe; notopodial furcate chaetae with handle smooth 9
8(7) Median parapodia with double aciculae both in notopodia and neuropodia; notopodial furcate chaetae with handle denticulated P. guadalupensis Amoureux, 1985; Caribbean Costa Rica
– Median parapodia with one acicula in notopodia and double aciculae in neuropodia; notopodial furcate chaetae with handle smooth P. levifuscina Perkins, 1984; North Carolina, USA
9(7) Median parapodia with one acicula, both in notopodia and neuropodia; palpophore longer than palpostyle P. capensis (Day, 1963); South Africa
– Median parapodia with double aciculae, both in notopodia and neuropodia; palpophore as long as palpostyle Podarkeopsis chinensis sp. nov.; Southeast coast of China

Acknowledgements

We thank Prof. Minggang Cai and Prof. Yongzhi Deng from Xiamen University, Mr Rongmao Li and Mr Huorong Chen from the Fisheries Resources Monitoring Center of Fujian Province for providing valuable survey information and logistic support. We also thank Prof. Shiqiang Zhou, Prof. Lizhe Cai, Kang Mei, Xiaoyu Zhao and Jingxiang Lin from Xiamen University, and Yuyao Li from Xiamen University Malaysia for collecting samples, and undergraduates Xiaolong Li, Penglong Liu, Dehao Meng, Haoyu Qi, and Xinghan Wei from Xiamen University and Quan Ma and Shen Zhong from Jimei University for genomic DNA extraction and PCR. We wish to show our sincere gratitude to the reviewers, Dr Pat Hutchings, and Dr Alexandra Rizzo, ZooKeys subject editor, Dr Christopher Glasby, and ZooKeys copy editors, Robert Forsyth and Zdravka Zorkova for their helpful comments and suggestions on the manuscript.

Additional information

Conflict of interest

The authors have declared that no competing interests exist.

Ethical statement

No ethical statement was reported.

Funding

This work was supported by the Postdoctoral Science Foundation of China (2021M691866), the Undergraduate Innovation and Entrepreneurship Training Programs of Xiamen University (202110384077), the MEL Outstanding Postdoctoral Scholarship, Lantau Conservation Fund of Hong Kong (RE-2020-22), Investigation on Marine Environment and Ecological Resources of Fujian Fishing Port Construction Project (2021), and Adjustment Funds Procurement Item of the Guangdong Daya Bay Aquatic Resources Provincial Nature Reserve Special Project (GDJR2021001).

Author contributions

ZW, CK and JWQ designed this project and jointly supervised this work. ZW and DY collected the samples. ST and DY conducted the morphological analyses, molecular experiments and data analyses. ST wrote the manuscript. All authors critically reviewed and approved the manuscript.

Author ORCIDs

Shan Tong https://orcid.org/0009-0008-4206-974X

Deyuan Yang https://orcid.org/0000-0003-3735-9909

Jian-Wen Qiu https://orcid.org/0000-0002-1541-9627

Caihuan Ke https://orcid.org/0000-0002-7288-3565

Zhi Wang https://orcid.org/0000-0003-1044-9226

Data availability

All of the data that support the findings of this study are available in the main text.

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