Research Article |
Corresponding author: Xiao-Chen Huang ( xchuang@ncu.edu.cn ) Corresponding author: Xiao-Ping Wu ( xpwu@ncu.edu.cn ) Academic editor: Graham Oliver
© 2023 Zhong-Guang Chen, Yu-Ting Dai, Shan Ouyang, Xiao-Chen Huang, Xiao-Ping Wu.
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:
Chen Z-G, Dai Y-T, Ouyang S, Huang X-C, Wu X-P (2023) Unveiling the identity of Diaurora Cockerell, 1903 (Bivalvia, Unionidae): morphology, molecular phylogenetics, and the description of a new species. ZooKeys 1173: 131-144. https://doi.org/10.3897/zookeys.1173.106148
|
The monotypic freshwater mussel genus Diaurora Cockerell, 1903 has long been enigmatic due to its rarity and morphological confusion with Acuticosta. In this study, we comprehensively redescribed Diaurora aurorea (Heude, 1883) through a detailed analysis of shell morphology and molecular phylogenetics of recently collected specimens. Moreover, a new species, Diaurora laeve sp. nov., was identified from the Fuyishui River, a tributary of the Zishui River in Shaoyang County, Shaoyang City, Hunan Province, China. Molecular phylogenetic analyses showed that D. aurorea and D. laeve sp. nov. were reciprocally monophyletic and formed a clade as sister to Schistodesmus. Our study underscores the necessity of further exploring the diversity of freshwater mussels in understudied small tributaries throughout China.
Changjiang River, freshwater mussel, morphology, phylogenetic analysis, taxonomy
Freshwater mussels, an important component of freshwater ecosystems (
Initially,
To address these taxonomic uncertainties, we analyzed the validity and systematic status of Diaurora using a combination of shell morphology and molecular phylogeny. Furthermore, we redescribed the enigmatic species Diaurora aurorea and described a new species, Diaurora laeve sp. nov., from the Zishui River of Hunan Province, China. Our study sheds light on the distribution, ecology, and protection of this distinct genus, and highlights the possibility of small Chinese tributaries harboring unique freshwater mussels.
Specimens were collected by hand net from the tributaries of the Changjiang River and the Jiulongjiang River from 2003–2022. These specimens were fixed in 95% ethanol, and some specimens were dissected for observation of the internal structure. Measurements were taken point-to-point with digital calipers recorded to the nearest 0.1 mm.
Genomic DNA was extracted from somatic tissues preserved in 95% ethanol using a TIANamp Marine Animals DNA Kit (Tiangen Biotech, China). The quality and concentration of the DNA were checked on 1% agarose gel electrophoresis and NanoDrop 2000 (Thermo Scientific, USA). F-type mitochondrial COI sequences, which are considered the barcode marker, were amplified using primers LCO22me2 (GGTCAACAAAYCATAARGATATTGG) and HCO700dy2 (TCAGGGTGACCAAAAAAYCA) (
GenBank accession numbers of sequences used in this study. * indicates the sequences newly obtained in this study.
Species | Locality | Accession number | References |
---|---|---|---|
Unioninae Rafinesque, 1820 | |||
Diaurora aurorea (Heude, 1883) 1 | Ji’an, Jiangxi, China | OQ829360* | This study |
Diaurora aurorea (Heude, 1883) 2 | Ji’an, Jiangxi, China | OQ829361* | |
Diaurora aurorea (Heude, 1883) 3 | Ji’an, Jiangxi, China | OQ829362* | |
Diaurora aurorea (Heude, 1883) 4 | Fuzhou, Jiangxi, China | OQ829366* | |
Diaurora laeve Chen, Dai, Huang & Wu, sp. nov. 1 | Shaoyang, Hunan, China | OQ829363* | |
Diaurora laeve Chen, Dai, Huang & Wu, sp. nov. 2 | Shaoyang, Hunan, China | OQ829364* | |
Diaurora laeve Chen, Dai, Huang & Wu, sp. nov. 3 | Shaoyang, Hunan, China | OQ829365* | |
Acuticosta chinensis (Lea, 1868) | Jiangxi, China | MG462921 |
|
Schistodesmus lampreyanus (Baird & Adams, 1867) | Jiangxi, China | MG463037 | |
Schistodesmus spinosus (Simpson, 1900) | Jiangxi, China | MG463046 | |
Schistodesmus sp. | Hunan, China | MG463043 | |
Unio pictorum (Linnaeus, 1758) | Europe | KC429109 |
|
Unio crassus Philipsson, 1788 | Poland | KY290446 |
|
Tchangsinaia piscicula (Heude, 1874) | Jiangxi, China | MG462977 |
|
Cuneopsis celtiformis (Heude, 1874) | Jiangxi, China | MG462964 | |
Cuneopsis heudei (Heude, 1874) | Jiangxi, China | MG462970 | |
Aculamprotula fibrosa (Heude, 1877) | Jiangxi, China | MG462909 | |
Nodularia douglasiae (Gray, 1833) | China | KX822653 |
|
Nodularia breviconcha Lee, Kim, Bogan & Kondo, 2020 | South Korea | MT020662 |
|
Inversiunio yanagawensis (Kondo, 1982) | Japan | MT020654 | |
Inversiunio reinianus (Kobelt, 1879) | Japan | MT020657 | |
Pseudocuneopsis sichuanensis Huang, Dai, Chen & Wu, 2022 | Sichuan, China | MZ540966 |
|
Pseudocuneopsis capitata (Heude, 1874) | Anhui, China | NC042469 |
|
Alasmidonta marginata Say, 1818 | USA | AF156502 | Graf and O’Foighil 2020 |
Lasmigona compressa (Lea, 1829) | USA | AF156503 | |
Anodonta anatina (Linnaeus, 1758) | Russia | KX822632 |
|
Pseudanodonta complanata (Rossmässler, 1835) | Ukraine | KX822661 | |
Lanceolaria gladiola (Heude, 1877) | Jiangxi, China | KY067441 | Unpublished |
Lanceolaria oxyrhyncha (Martens, 1861) | Japan | MT020648 |
|
Cristaria plicata (Leach, 1814) | Jiangxi, China | MG462956 |
|
Lepidodesma languilati (Heude, 1874) | Jiangxi, China | MG463015 | |
Sinanodonta woodiana (Lea, 1834) | China | KX822668 |
|
Beringiana beringiana (Middendorff, 1851) | Japan | MT020557 |
|
Pletholophus tenuis (Gray, 1833) | Vietnam | KX822658 |
|
Anemina arcaeformis (Heude, 1877) | Jiangxi, China | MG462936 |
|
Amuranodonta kijaensis Moskvicheva, 1973 | Russia | MK574204 |
|
Parreysiinae Henderson, 1935 | |||
Coelatura aegyptiaca (Cailliaud, 1823) | Egypt | KJ081162 |
|
Indonaia andersoniana (Nevill, 1877) | Myanmar | MF352275 |
|
Parreysia nagpoorensis (Lea, 1860) | India | JQ861229 | Unpublished |
Gonideinae Ortmann, 1916 | |||
Pronodularia japanensis (Lea, 1859) | Japan | LC505454 |
|
Lamprotula leaii (Gray, 1833) | Jiangxi, China | MG462996 |
|
Ambleminae Rafinesque, 1820 | |||
Lampsilis siliquoidea (Barnes, 1823) | USA | MH560773 | Unpublished |
Quadrula quadrula (Rafinesque, 1820) | USA | HM230409 | |
Margaritiferidae Henderson, 1929 | |||
Margaritifera dahurica (Middendorff, 1850) | Russia | KJ161516 |
|
Gibbosula rochechouartii (Heude, 1875) | Jiangxi, China | MG463022 |
|
Sequences were aligned using MEGA v. 6.0 (
NCU Nanchang University (Nanchang, Jiangxi, China)
NZMC National Zoological Museum of China (Beijing, China)
YHC Collection of Mr Hao Yang (Xiamen, Fujian, China)
A total of 43 mitochondrial COI sequences from 38 unionoid species were utilized in the phylogenetic analyses (Table. 1). Phylogenetic analyses revealed ML and BI trees with largely consistent topologies (Figs
Family Unionidae Rafinesque, 1820
Subfamily Unioninae Rafinesque, 1820
Unio auroreus Heude, 1883, by original designation.
Shell small size, symmetric, flat, sub-glossy, triangular-ovate to reniform, orangish to brownish, with broken blackish-green rays. Zigzag sculpture present. Posterior ridge absent.
Aurora Simpson, 1900 was originally described as a subgenus of Parreysia based on shell morphology.
Holotype : USNM472411, Ning-kouo hien [宁国县], Kien-té hien [建德县], China. NZMC FM00732, Yuanjiang River [沅江], Hunan Province [湖南省], China. SMF24000a–b, Yütanchiao [玉潭桥], Hunan [湖南], China, 28°15′7″N, 112°33′45″E.
22_NCU_XPWU_DA01–02, Fuhe River [抚河], Fuzhou City [抚州市], Jiangxi Province [江西省], China, 27°53′57″N, 116°34′03″E, collected by Zhong-Guang Chen, Yu-Ting Dai, Chen-Chen Jia & Ying-Ying Zhang in September 2022. 22_NCU_XPWU_DA03–15, Ganjiang River [赣江], Jian City [吉安市], Jiangxi Province [江西省], China, 27°12′39″N, 115°09′44″E, collected by Zhong-Guang Chen & Zheng-Jie Lou in November 2022. YHC0028001, Jiulong River [九龙江], Fujian Province [福建省], China, collected by Hao Yang in 2003.
Shell triangular-ovate; posterior margin obliquely arc-shaped. Periostracum with straight broken blackish-green rays. Zigzag sculpture presented on all over the shell surface.
Shell (Figs
Length 32.0–41.3 mm, height 20.5–26.0 mm, width 12.4–17.2 mm.
Soft anatomy
(Fig.
Soft anatomical characters of Diaurora A Diaurora aurorea, 22_NCU_XPWU_DA15 B Diaurora laeve sp. nov., 22_NCU_XPWU_DL50. aam, anterior adductor muscle; pam, posterior adductor muscle; ea, excurrent aperture; ia, incurrent aperture; pia, papillae of the incurrent aperture; pea, papillae of the excurrent aperture; ig, inner gills; og, outer gills; m, mantle; lp, labial palps; vm, visceral mass; f, foot.
金黄蚌 (Pinyin: jin huang bang).
Scattered in the middle and lower Changjiang River basin and the upper Jiulongjiang River, including Anhui Province, Jiangxi Province, Hunan Province and Fujian Province (Fig.
The rarity of D. aurorea has been seriously underestimated for a long time due to the common misidentification of museum material. Upon examination of museum specimens, it has been discovered that specimen NZMC10542 in the National Zoological Museum of China and specimens 15_NCU_XPWU_AA01–11 in Nanchang University were actually Acuticosta chinensis. Since its original description, only a handful of additional specimens of D. aurorea have been correctly identified. It has always been shrouded in mystery as there are hardly any photographs of specimens other than the type specimen. The new specimens examined in this study indicate that it is far more widespread than previously recorded. However, the habitats of D. aurorea are severely fragmented and the population size is very small. Therefore, it requires more attention and protection in the future.
Holotype: 22_NCU_XPWU_DL01, Zishui River [资水], Shaoyang County [邵阳县], Shaoyang City [邵阳市], Hunan Province [湖南省], China, 26°59′27″N, 111°16′10″E, collected by Zhong-Guang Chen & Zheng-Jie Lou in November 2022; Paratypes: 22_NCU_XPWU_DL02–100, other information same as holotype.
Shell reniform. Periostracum with irregular broken blackish-green rays. Zigzag sculpture only presented in umbo area.
Shell (Figs
Holotype : length 41.8 mm, height 29.1 mm, width 17.0 mm; Paratypes: length 27.4–45.0 mm, height 17.6–30.8 mm, width 11.0–17.6 mm.
Soft anatomy
(Fig.
The specific name laeve is made from the Latin laeve for smooth, an adjective, alluding to the smoother shell surface of this species.
平滑金黄蚌 (Pinyin: ping hua jin huang bang).
Diaurora laeve sp. nov. is known from the type locality only (Fig.
The placement of the new species in Diaurora is supported by both morphology and molecular phylogenetic analysis. Diaurora laeve sp. nov. can be easily distinguished from D. aurorea by its reniform shell, smaller zigzag sculptured area, and irregular rays on the shell. The different habitat preferences of Diaurora laeve sp. nov. and D. aurorea may have led to their differentiation. Diaurora aurorea is commonly found in the middle reaches of sandy substrate tributaries, while Diaurora laeve sp. nov. prefers to inhabit the upper reaches of pebbly substrate tributaries. In recent years, with more in-depth investigations and field surveys, new freshwater mussel species such as Inversidens rentianensis Wu & Wu, 2021 and Pseudocuneopsis sichuanensis Huang, Dai, Chen & Wu, 2022 have been discovered in small tributaries of China (
We thank Zheng-Jie Lou (Hangzhou), Chen-Chen Jia (Nanchang University) and Ying-Ying Zhang (Nanchang University) for assistance in specimen collection; Hao Yang (YHshells, Xiamen) and Qing Zhang (YHshells, Xiamen) for assistance in specimen examination.
The authors have declared that no competing interests exist.
No ethical statement was reported.
This study was supported by the National Natural Science Foundation of China under Grant No.31772412 and No.32100354.
Zhong-Guang Chen, Yu-Ting Dai, Xiao-Chen Huang & Xiao-Ping Wu designed the study. Zhong-Guang Chen & Yu-Ting Dai collected the specimens. Zhong-Guang Chen & Yu-Ting Dai examined the specimens, performed morphological comparisons and conducted molecular analysis. All authors prepared the manuscript, read and approved the final version.
Zhong-Guang Chen https://orcid.org/0000-0003-2689-3321
Yu-Ting Dai https://orcid.org/0009-0001-5856-3987
Xiao-Chen Huang https://orcid.org/0000-0002-0242-3571
Xiao-Ping Wu https://orcid.org/0000-0002-8037-5640
All of the data that support the findings of this study are available in the main text.