Biodiversity Data Journal :
Taxonomy & Inventories
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Corresponding author: Lingfeng Kong (klfaly@ouc.edu.cn)
Academic editor: Sérgio Ávila
Received: 25 Apr 2023 | Accepted: 22 Jun 2023 | Published: 07 Jul 2023
© 2023 Lu Qi, Biyang Xu, Lingfeng Kong, Qi Li
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:
Qi L, Xu B, Kong L, Li Q (2023) Checklist of the micromolluscs in the intertidal zone of the Yellow Sea and Bohai Sea, China. Biodiversity Data Journal 11: e105444. https://doi.org/10.3897/BDJ.11.e105444
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The diversity of the sedimentary environment and molluscs is rich in the intertidal zone of the Yellow Sea and Bohai Sea. At present, many of the investigations focus on macromolluscs, while the diversity of micromolluscs is seriously underestimated.
In this study, the survey of micromolluscs was carried out in the intertidal zone of the Yellow Sea and Bohai Sea. The collection and preservation of micromolluscs, as well as the preparation methods of morphological characteristic structures by scanning electron microscopy (SEM) were explored. A total of 20 species were described in this survey. These can be assigned to 16 families, four orders (Vetigastropoda (1), Caenogastropoda (10), Heterobranchia (5) and Autobranchia (3)) and two classes (Gastropoda (17), Bivalvia (3)).
biodiversity, description, mollusca, morphology
Molluscs are one of the largest groups of marine benthos, with a huge variety of life strategies. In marine ecosystems, molluscs occupy different trophic levels, from filtrators and phytophages to predators and parasites. Due to their high diversity and widespread distribution, they have been widely recorded in taxonomic monographs. Recent examples of taxonomic monographs from the Western Pacific Region included
Micromolluscs are important components of molluscs and play an important role in biodiversity assessments. As micromolluscs usually require specific collecting/sorting attention and have a reputation for presenting formidable taxonomic difficulties, they are often overlooked in biodiversity surveys, resulting in a gross underestimation of mollusc diversity. In a biodiversity survey of New Caledonia, the micromolluscs account for approximately one-third (33.5%) of all identified mollusk species, with the largest size class being 1.9–4.1 mm (
The diversity of the sediment environment and molluscs is rich in the intertidal zone of China. However, much of the literature focuses on macromolluscs that can be collected by hand-picking in the field. Only
Sampling was carried out in the intertidal zone of the Yellow Sea and Bohai Sea from September 2017 to December 2019 (Fig.
Name |
Abbreviation |
Area and Geographic Data |
Date of Collection |
Tangshan |
TS |
|
20.10.2017 |
Dongying |
DY |
|
24.06.2018 |
Yantai |
YT |
|
12.08.2018 |
Weihai |
WH |
|
03.06.2019 |
Qingdao |
QD |
|
09.07.2019 |
Ganyu |
GY |
|
20.09.2019 |
Shell grit or shell sand
The sediments usually contain mainly empty shells and certain species should be divided into size fractions by using graded sieves (e.g. 10, 5, 2.5, 1.0 and 0.4 mm mesh size). If there is a need to collect all adult species, the 0.4 mm sieve is suitable.
Algal samples
Algae are one of the most important habitats for micromolluscs. After the algae are collected on-site, it should be placed in a bucket or ‘zip-lock’ bag and then the bucket or bag should be shaken violently. The algal material is then removed and the sample is allowed to settle briefly. The water can then be gently decanted, being run through a sieve to catch any floating molluscs.
Rock
The upper and undersides of rocks are very different environments. Some micromolluscs may be attached to the algal films or turf on the rock surface. These rocks can be scrubbed with a brush in a bucket. Then the residue in the bucket is collected into the sample bottle.
Specimens for anatomical study were stored in formalin, whereas for molecular work, strong (> 95%) ethanol or RNALater are the best preservatives. All samples were brought back to the laboratory for further processing. All the material collected has been deposited in the Laboratory of Shellfish Genetics and Breeding (LSGB), Fisheries College, Ocean University of China, Qingdao, China. Morphological identification of the species was carried out mainly through the identification book from
Traditional barcoding gene COI was analysed for most specimens to verify identification. Total genomic DNA was extracted from entire animals with the TIANamp Marine Animals DNA Kit (Tiangen Biotech, Beijing, China), according to the manufacturer’s protocol and stored at -4°C for short-term use. Amplification of partial sequences of mitochondrial COI was amplified by a polymerase chain reaction using the primers from
Species used in this study, species name and taxonomic ranks, GenBank accession numbers, locality of collection and Date of Collection.
Family |
Species name |
Genbank |
Locality |
Date of Collection |
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Gastropoda |
Vetigastropoda |
Trochidae |
Lirularia iridescens (Schrenck, 1863) |
MT254075 |
Weihai |
2018 |
Caenogastropoda |
Litiopidae |
Alaba picta (A. Adams, 1861) |
MT254074 |
Qingdao |
2018 |
|
Barleeiidae |
Barleeia angustata (Pilsbry, 1901) |
MT254076 |
Weihai |
2018 |
||
Barleeia sp. |
MT254077 |
Qingdao |
2017 |
|||
Iravadiidae |
Iravadia elegantula (A. Adams, 1861) |
MT240257 |
Dongying |
2017 |
||
Stenothyridae |
Stenothyra glabra A. Adams, 1861 |
MN548735 |
Ganyu |
2019 |
||
Assimineidae |
Assiminea estuarina Habe, 1946 |
MT240258 |
Weihai |
2019 |
||
Rissoidae |
Alvania concinna A. Adams, 1861 |
MT240259 |
Weihai |
2018 |
||
Tornidae |
Pseudoliotia pulchella (Dunker, 1860) |
- |
Tangshan |
2018 |
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Littorinidae |
Peasiella habei D. Reid & Mak,1998 |
MT823260 |
Qingdao |
2019 |
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Lacuna carinifera (A. Adams, 1853) |
MT823257 |
Weihai |
2018 |
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Heterobranchia |
Tornatinidae |
Acteocina fusiformis (A. Adams, 1850) |
- |
Tangshan |
2019 |
|
Retusidae |
Pyrunculus tokyoensis Habe, 1950 |
- |
Tangshan |
2019 |
||
Pyramidellidae |
Brachystomia bipyramidata(Nomura,1936) |
MT823256 |
Qingdao |
2018 |
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Odostomia subangulata A. Adams, 1860 |
MT254072 |
Qingdao |
2018 |
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Turbonilla osyuensus Nomura, 1936 |
- |
Tangshan |
2018 |
|||
Rissoellidae |
Rissoella elatior (Golikov, Gulbin & Sirenko, 1987) |
- |
Tangshan |
2019 |
||
Bivalvia |
Autobranchia |
Lasaeidae |
Lasaea undulata (A. A. Gould, 1861) |
MT254080 |
Weihai |
2018 |
Kelliellidae |
Alveinus ojianus (Yokoyama, 1927) |
- |
Tangshan |
2019 |
||
Arcidae |
Bentharca sp. |
- |
Tangshan |
2019 |
Specimens can be immersed for one to two minutes in strong commercial bleach to remove the periostracum. The soaked shells were placed in a centrifugal tube with neutral detergent and cleaned by ultrasound. The cleaning time depends on the amount of dirt on the shell surface. After sonication, shells should be washed in distilled water preferably two or three times. After the last wash, the water drops should be removed with a paper towel and the specimen air-dried. The clean shells were attached to conductive glue in the direction of the standardized views and then sputtered with gold. The thickness of the metal coating is 1-10 nm; however, even excessive coating will not interfere with the detail in a normal shell. The operating tool was TESCAN VEGA3 scanning electron microscope (SEM).
Shell minute (2.5±0.26 mm in width, 2.2±0.15 mm in length), ovato-conica. Whorls 4-5, spire low, body whorl rather ventricose (Fig.
Found on seagrass between tidal and shallow waters.
Yellow Sea of China; Japan Sea, South Kurile Islands.
L. iridescens was recorded by
Shell small (8.5±0.34 mm in height, 4.5±0.18 mm in width), ovate-conica, thin, fragile, translucent, whorls about 8, less inflated, spire high, body whorl inflated (Fig.
Found on seagrass between tidal and shallow waters.
From Liaoning to Shandong coasts of China; Japan; Australia.
Alaba picta with obvious morphological variance in colour, aperture, shell length and sculpture (
Shell minute (4.3±0.76 mm in length, 1.2±0.26 mm in width), conical, depressed or auricular (Fig.
Lives on intertidal sandy mud, algae.
China, Japan.
Stenotis lois (Yen, 1936) is very similar to Lacuna carinifera (A. Adams, 1853), but the aperture is wider, with angulate periphery on the underside of the outer lip, the umbilicus more open. This study thinks Stenotis lois (Yen, 1936) is the larva of Lacuna carinifera (A. Adams, 1853) and is a synonym.
Shell minute (2.5±0.18 mm in length, 1.3±0.09 mm in width), elongate conical, solid (Fig.
Lives on algae in intertidal and sublittoral zones.
China, Japan, Australia.
The species originally belonged to Rissoidae. Rissoina dunedini Grabau & S. G. King, 1928 and Rissoina nelsoni Grabau & S. G. King, 1928 were the synonyms of this species (
Shell minute (1.2±0.42 mm in width, 1.8±0.13 mm in length), conic to ovate-conic, dark brown, smooth or with weak axial microsculptures and rather solid, periphery weak convex to angled (Fig.
Lives on algae in intertidal and sublittoral zones.
China
Barleeia sp. very similar to Barleeia angustata (Pilsbry, 1901), but the aperture is open.
Shell minute (3.0±0.22 mm in length, 1.6±0.14 mm in width), elongate conical, stout (Fig.
Brackish water, on muddy flats and under rocks in estuary at river mouth.
Korea, China, Japan.
The Iravadia includes the subgenera Fluviocingula Kuroda & Habe, 1954, Pseudomerelina Ponder, 1984 and Pseudonoba O. Boettger, 1902. The original description from the species Onoba elegantula A. Adams, 1861. At present, the Iravadia elegantula (A. Adams, 1861) has been accepted as Fluviocingula elegantula (A. Adams, 1861).
Shell minute (2.1±0.14 mm in length, 1.5±0.07 mm in width), ovate-conic, rather thick, dorso-ventrically compressed, with rounded to angled inflation of last whorl (Fig.
Inhabiting the surface of mud flats or attaching to the under surface of floating leaves in freshwater estuaries.
Yellow Sea and Bohai Sea of China, Korea and Japan.
The type locality of Stenothyra glabra A. Adams, 1861 is “estuary of the Pei-ho, North China”, which is on the coast of the Bohai Sea. One of the localities in this study, Yellow River Estuary, is adjacent to the type locality. Moreover, the shells exhibit remarkable similarity in terms of size, shape, and microsculpture when compared to the descriptions provided by
Shell minute (2.2±0.36 mm in length, 1.5±0.08 mm in width), globose-conic, solid (Fig.
Lives on mud bottoms in brackish water areas of estuaries.
China, Japan.
The genus Assiminea H. & A. Adams, 1865 is cosmopolitan, but most of them are from the Indo-pacific Region. A. estuarina is rarely found in China. The shell of this species is similar to A. hiradoensis Habe, 1942, but there are some differences between them. Each whorl of A. estuarina is more convex than A. hiradoensis. The height of the spire of A. hiradoensis is higher.
Shell minute (4.5±0.41 mm in length, 2.4±0.11 mm in width), elongate conical (Fig.
Lives in intertidal areas in sheltered bays on seaweed.
China, Japan and Korea.
The trait of the genus Alvania Risso, 1826 is that the teleoconch is ovate-conic to elongate-conic, with clathrate sculpture or spiral sculpture (
Shell minute (1.3±0.19 mm in length, 3.1±0.16 mm in width), depressed conical, round pie, solid (Fig.
Under rocks on sandy gravel bottoms in intertidal zones in sheltered areas.
China, Japan.
Pseudoliotia Tate, 1898 is characterised by a depressed conical shell with strong axial and spiral ribs on its surface. P. pulchella is similar to P. astericus, but much larger, lower in shell height and with relatively weak axial ribs.
Shell minute (3.0±0.28 mm in length, 2.4±0.09 mm in width), depressed conical, thick, stout; outline domed (Fig.
The species is abundant in crevices and amongst barnacles in the middle and upper eulittoral zone, on sheltered and moderately exposed rocky shores; on exposed shores, it shows a preference for surfaces protected from wave action.
China, Korea, Taiwan, Japan.
This species is variable in conspicuous features of the shell including colour, spire profile and sculpture, but consistent characteristics are the row of dark spots above the periphery, which extend on to the pale peripheral keel, the darker and often black spire whorls and the prominent keel at the periphery.
Shell minute (2.5±0.15 mm in length, 0.9±0.08 mm in width), cylindrical to fusiform, thick, solid, with fine and indistinct spiral grooves (Fig.
Found on sandy and mud bottoms in intertidal seagrass bed.
Bohai Sea in China, Japan, South African.
Shell cylindrical or fusiform, spire conspicuous, apex papillated, suture channelled, columella callous, with a single fold in the genus Acteocina Gray, 1847 (
Shell minute (3.0±0.34 mm in length, 1.3±0.11 mm in width), pyriform, thin, white, polished (Fig.
Found on sandy and mud bottoms in intertidal seagrass beds.
China and Japan.
P. tokyoensis is similar to P. phiala, but differs from P. phiala in having distinct spiral grooves overall.
Shell minute (3.2±0.27 mm in height, 1.5±0.34 mm in width), oval conical, moderately thick, translucently milky-white, solid (Fig.
Sucking body fluid of Crassostrea gigas on rocks in intertidal zones.
North of China, Japan.
The genus Brachystomia Monterosato, 1884 is very similar to Odostomia spp. in shell characters, but differs in the protoconch turning down on the teleoconch apex, attaching to other molluscs when alive (
Shell minute (5.0±0.12 mm in height, 2.3±0.03 mm in width), conical, milky-white, moderately thick, solid (Fig.
Sucking body fluid of Crassostrea gigas on rocks in intertidal zones.
North of China, Japan.
Megastomia tenera (A. Adams, 1860) very similar to Odostomia subangulata A. Adams, 1860 in shell characters, but differs in having palatal ridges in the inner lip.
Shell minute (3.8±0.13 mm in height, 1.0±0.21 mm in width), towered, moderately solid, white (Fig.
Found on sandy mud bottoms of seagrass beds.
Bohai Sea of China, Japan.
Chemnitzia osyuensis (Nomura, 1936) is the type specimen and a synonym. Very similar to T. gracilenta, but differs in the protoconch rotated right (
Shell minute (1.5±0.12 mm in height, 0.88±0.06 mm in width), elongate oval, thin, vitreous, fragile, translucent (Fig.
Living on seagrass.
China, Japan, Russia.
The shell characteristics of the genus Rissoella are thin; vitreous and soft parts can be seen through it. As some species are similar in morphology, many species are misidentified or undescribed. In this study, our sampled material agrees with the original description of this species (
Shell small (2.7±0.15 mm in length, 1.9±0.11 mm in height), elongate-ovate, thin, fragile (Fig.
Attached to the byssus of the septifer and the roots of seaweeds between tidal marks.
Yellow Bay (Shandong Province) of China, Japan.
Lasaea consists of small pelecypod species, the largest of which attains a size of about 8 mm in length; adult specimens of the smaller species are about 2 mm long. In general, these shells are quadrangular in outline; they are equivalved, but inequilateral, the anterior end being the longer (
Shell minute (1.1±0.17 mm in length, 1.0±0.22 mm in height), triangular-ovate, inflated, equivalved (Fig.
Found on sandy mud bottoms in upper sublittoral zones.
Yellow Sea and Bohai Sea of China, southern Japan.
Spaniodon Reuss, 1867 was considered a senior synonym of Alveinus Conrad, 1865, containing only Alveinus miliaceus (Issel, 1869) and Alveinus ojianus (Yokoyama, 1927) in WoRMS. A. miliaceus is very similar to A. ojianus in shell characters, but differs in the cardinal tooth. The cardinal teeth bifurcate into two lamellae (
Shell minute (2.3±0.02 mm in length, 1.5±0.04 mm in height), elongate squarish, thin, moderately inflated (Fig.
Found on sandy mud bottoms in upper sublittoral zones.
Bohai Sea of China.
This species is very similar to Bentharca spp. in shell characters including radial riblets and is covered with lamellate epidermis at interstices, cardinal plate and umbo.
A total of 20 species were described in this survey (Table
This study described the diversity of common micromolluscs from the Yellow Sea and Bohai Sea in China. A total of 20 species were collected, belonging to 16 families and 16 genera of Gastropoda and 3 families and 3 genera of Bivalve, respectively. The statistics show that Caenogastropoda has the highest species diversity, which should be attributed to two essentially micromollusc groups, Rissooidea and Truncatelloidea (Fig.
The statistical chart of micromolluscs diversity and habitat. A The numbers in front of the species names indicate the number of collected specimens. Different colours represent different orders. B The percentage of species in different habitats. Different colours represent different habitats.
In terms of morphology, this study analysed the surface characteristics of the shells in detail by taking SEM images of the shells and carried out morphological identification and description, but there are still many undetermined species and, due to the limited amount of sample, a further morphological study could not be carried out. Meanwhile, this also means that there are still many micromolluscs to describe.
According to the survey, it is found that most of the micromolluscs inhabit seagrass (25%), sandy mud bottom (25%), algae (15%), mud and under rocks (5%) and others habitats (respectively 10%) (Fig.
This study was supported by the Hainan Provincial Joint Project of Sanya Yazhou Bay and Technology City Grant 320LH019, the National Natural Science Foundation of China under Grant 31772414, and the Fundamental Research Funds for the Central Universities under Grant 201964001. We thank Dr. Takenori Sasaki from the University of Tokyo, for his advice on the morphological research.
All authors were involved in collecting the animals. L. Q. analysed the material, designed the figure and wrote the manuscript. All authors read and approved the final manuscript.