Nassarius sinarum (Philippi, 1851)

Cho, Sungha, Yang, Inho, Khim, Jong Seong & Park, Jinsoon, 2023, First confirmed report of Nassarius sinarum (Mollusca, Gastropoda) in Korea, Biodiversity Data Journal 11, pp. 99661-99661 : 99661

Nassarius sinarum (Philippi, 1851)

Synonyms and Combinations

Buccinum sinarum ( Philippi 1851: v. 8, p. 63)

Nassa (Niotha) sinarum ( Philippi (1851): v. 8, p. 63); Tsuchiya (2017): p. 910-917; Okutani (2017): p. 1375.

Nassarius (Zeuxis) sinarus ( Philippi (1851): v. 8, p. 63); Cernohorsky (1984): v. 14, p. 289, pl. 31, figs. 10-11; pl. 32, fig. 1; Tamaki et al. (2002): v. 8, no. 2, p. 63-81; Lutaenko et al. (2013): p. 75.

Nassarius (Tritonella) semiplicatus ( A. Adams (1852): no. 19, p. 107); Liu (2008): p. 1267.

Nassarius (Zeuxis) semiplicatus ( A. Adams (1852): no. 19, p. 107); Zhang and Yang (2010): v. 41, no. 5, p. 791-5.

Nassarius semiplicatus ( A. Adams (1852): no. 19, p. 107); Zhang and Yang (2010): v. 41, no. 5, p. 791-5.

Zeuxis semiplicata ( A. Adams (1852): no. 19, p. 107); A. Adams (1852): v. 24, p. 233, pl. 23, figs. 164; Cernohorsky (1984): v. 14, p. 154.

Material examined

On 16 June 2022, two live specimens were collected from the Yeongsan River estuary at Jeollanam-do, Korea (34°46'48"N, 126°26'31"E), located at 219 Daeburyeok-ro Samho-eup, Yeongam-gun (Fig. 1 ). The environmental conditions at the time of collection included a water temperature of 24.5°C, dissolved oxygen (DO) levels of 5.69 mg/l, salinity of 33.24 practical salinity units (PSU) and a pH of 8.37. The collector responsible for this sampling was Sungha Cho.

Description

Sample A, exhibiting a shell length of 14 mm and Sample B, with a shell length of 15 mm, are not fully developed individuals in comparison to the known maximum size of N. sinarum, which reaches up to 20 mm (Fig. 2 ). The undeveloped outer lip at the base further indicates that these specimens might be juveniles or subadults (Fig. 3 ). Both individuals A and B seem to be at the same developmental stage. Samples A and B, collected in this study, were photographed in both apertural and dorsal views to facilitate morphological comparisons. Sample C, collected in China, is depicted in apertural and dorsal views and is considered a juvenile shell, similar in growth stage to Samples A and B from Korea, due to the absence of a developed thick outer lip ( Lynio 2023). Nonetheless, the axial ribs become progressively thinner as they approach the outer lip, suggesting that the specimen may be at a more mature developmental stage. Specimen D, collected in Japan, appears to be an adult shell, based on morphological features observed in apertural and dorsal views and exhibits a greyish-brown hue with pale spiral bands ( Magokorogai 2013). The axial ribs are obtuse, spaced and knobbly at the shoulders, but become obsolete towards the base. The aperture is white inside and the callus on the columellar lip is demarcated, bearing one tooth at the posterior end. The anal canal is narrow and the inner wall of the outer lip is denticulated. In contrast, Korean Samples A and B, believed to be juveniles, display an aperture with uniform colouration and lack callus and tooth formation throughout the shell. Specifically, in the adult body whorl, the axial ribs weaken towards the outer lip, ultimately becoming nearly smooth, which is a key distinguishing feature of N. sinarum, yet not observed in juvenile shells. Limited photographs of N. sinarum are available for comparison and those that exist are fragmentary.

Distribution

Initially, N. sinarum was thought to be exclusive to the Yangtze River in China ( Cernohorsky 1984). However, in 2004, its presence was later documented in Japan, where it was classified as an alien species ( Mito and Uesugi 2004). Although Hong et al. (2010) reported observing it in Suncheon Bay, Korea in June 2009, the species' introduction remained uncertain due to a lack of corroborating data. This study documents the collection of live N. sinarum specimens from the Yeongsan River estuary in Korea, confirming that the species now inhabits Korea, China and Japan.

Molecular data

The sequence files were submitted to the NCBI and assigned accession numbers: OP693482 (660 bp) for COI and OP719775 (372 bp) for H3. The NCBI Basic Local Alignment Search Tool (BLAST) analysis demonstrated that our N. sinarum COI sequence matches that previously registered for N. sinarum, exhibiting 98.48-99.69% sequence similarity (Table 1 ). N. succinctus was the nearest species, with 93.86% percent similarity. Our sequence's similarity as N. sinarum was further confirmed by a Maximum Likelihood tree, which was analysed for percentage similarity with the top 10 sequences retrieved from NCBI BLAST. Outgroups (Volutharpa perryi, Buccinum pemphigus and Neptunea cumingi) were included to improve clustering and branch support ( Yang et al. 2019). To bolster the robustness of the phylogenetic analysis, we incorporated an additional 29 species from the Nassarius. The close clustering of N. sinarum within the phylogenetic COI tree suggests species consistency; no sequence differences were observed within species or between countries (Fig. 4 ). An H3 phylogenetic analysis was performed for more accurate identification, using the same conditions as were used for the COI analysis. As the H3 region of N. sinarum is novel to the NCBI database, species-level comparisons were not feasible. The H3 phylogenetic tree encompassed difficulties in distinguishing amongst species within the same genus (Fig. 5 ). Thus, it appears that H3 is not a suitable marker for differentiating species within the Nassarius.

Ecology and habitat

Nassarius, commonly known as nassa mud snails (USA) or dog whelks (UK), is a genus of small to medium-sized marine gastropod molluscs in the Nassariidae characterised by their scavenging behaviour. These shelled gastropods inhabit mud flats and sand flats, have a global distribution and have a diverse habitat range that spans from the intertidal zone to deep waters (depths of at least 1000 m) in temperate, subtropical, tropical and cold-water environments. Nassarius species are highly active scavengers, feeding on crabs and carrion, such as dead fish. They often burrow into marine substrates, waiting with only their siphon exposed until detecting nearby food sources. Consistent with these ecological traits, N. sinarum inhabits both sandy and muddy mudflats and occupies various environments within the intertidal zone ( Okutani 2017).

Remarks

Iwasaki et al. (2004) documented damage related to the presence of N. sinarum, including predation on fish (e.g. gobies) captured in fishing nets, in Japan's Saga and Kumamoto Prefectures. The species is believed to have been introduced to Japan through the importation of edible shellfish from China. Currently classified as an alien species in Japan, N. sinarum 's status as a harmful invasive species is still under evaluation by Japan's IAS ( Mito and Uesugi 2004). Nevertheless, purported negative impacts on the fishing industry suggest that this species warrants attention and monitoring.

Figures

Figure 1. Sample collection site details. A The fine-scale location of the collection site was obtained using Ocean Data View (Schlitzer R, 2015, http: // odv. awi. de); B Photograph of the sampling location at the Yeongsan River, taken in June 2022 and provided by Sungha Cho.

Figure 2. Morphological images of Nassarius sinarum from Korea, China and Japan. A & B Specimens collected alive in the estuary at the mouth of the Yeongsan River in Korea (this study) and considered to be juvenile shells; apertural and dorsal views were photographed; C Specimen collected alive in China; D Specimen collected alive in the mudflats of Japan; morphological features of the apertural and dorsal views suggest it is an adult shell. Scale bars for A and B are 5 mm; scale bars for C and D are not provided. For original images and data, consult Suppl. material 1.

Figure 3. Scanning electron microscope images of the shell of Nassarius sinarum Specimen B, collected in this study. A Morphology, characterised by the absence of a developed callus and tooth in the aperture; B Axial ribs exhibiting a consistent appearance as they extend to the outer lip; C Body whorl sculpture; D Protoconch. Scale bar A & B = 2 mm, C = 1 mm, D = 200 μm. For additional scanning electron microscopy images, please refer to Suppl. material 1.

Figure 4. Maximum Likelihood tree of COI sequences of Nassarius sinarum collected in Korea. Bars represent genetic distances, letters preceding scientific names are NCBI accession numbers. A phylogenetic tree analysis conducted with the COI region demonstrates that N. sinarum has a distinctive species-indicative COI sequence.

Figure 5. Maximum Likelihood tree of H 3 sequences of Nassarius sinarum collected in Korea. Bars represent genetic distances, letters preceding scientific names are NCBI accession numbers. A phylogenetic tree analysis conducted with the H 3 region reveals that H 3 sequences of N. sinarum cannot be used to clearly distinguish it from other Nassarius species.