New Record of Geoduck Clam Collected from the East Coast of South Korea and Its Reproductive Characteristics
1
Marine Bio-Resources Research Unit, Korea Institute of Ocean Science & Technology (KIOST), Busan 49111, Republic of Korea
2
Division of Zoology, Honam National Institute of Biological Resources, Mokpo 58762, Republic of Korea
3
GABI Co., Ltd., Gangneung 25440, Republic of Korea
*
Author to whom correspondence should be addressed.
J. Mar. Sci. Eng. 2023, 11(4), 776; https://doi.org/10.3390/jmse11040776
Submission received: 10 March 2023
/
Revised: 29 March 2023
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Accepted: 31 March 2023
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Published: 3 April 2023
(This article belongs to the Special Issue Taxonomy, Biodiversity, and Distribution of Marine Invertebrates)
Abstract
:Geoduck clams are important commercial marine resources in Southeast Asia. However, the complete mitochondrial genome of the native geoduck clam in South Korea has not been reported yet. This study reports a geoduck clam collected from the east coast of South Korea. Based on its morphological characteristics and molecular data, the geoduck clam was identified as Panopea sp. belonging to the bivalve family Hiatellidae. We determined the complete mitochondrial genome of this species and investigated the seasonal reproductive pattern for monthly changes in sex ratio, gametogenesis, and reproductive cycle from September 2019 to August 2020. The total length of the complete mitochondrial genome sequence is 16,006 bp, containing 13 protein-coding, 22 transfer RNA, 2 ribosomal RNA, and a control region (D-loop). A molecular phylogenetic comparison with 10 bivalve species showed that the geoduck clam specimen belongs to the family Hiatellidae, clustering with Panopea abrupta Chinese strain, P. generosa, and P. globosa. The gametogenesis of the geoduck clam was identified in six stages by histological analysis. The sex ratio was biased towards males from May 2019 to July 2019, the main spawning activity from the frequency of the gonads with ripe and spent stages occurred from October 2018 to April 2019, and there was no clear pattern of spawning peaks from May to August 2019 with gonads developed asynchronously between both sexes. This is the first study to report new records of the genus Panopea based on the complete mitochondrial genome and to examine the seasonal reproductive pattern of the native geoduck clam Panopea sp. in South Korea, providing valuable information for its sustainable management in South Korea.
1. Introduction
The genus Panopea (geoduck clams) is one of the largest burrowing bivalves in the world and one of the longest-lived animals, with a reported record age of 168 years [1]. These clams were known to be a cosmopolitan species during the Triassic, accommodating 150 fossil species, and 10 living species were distributed in temperate to subtropical waters [2]. In East Asia, two Panopea species are commonly found in coastal subtidal regions: P. abrputa in China [3] and P. japonica in Japan and Korea [2,4,5].
Geoduck clams have been widely cultivated as commercial marine fisheries resources in Southeast Asia and the southeast coastal region of China. Currently, China is one of the largest markets for geoduck clams [6]. However, despite their high commercial importance, natural geoduck clam populations have declined owing to rising market demand and overfishing [7,8]. In Korea, although previous studies on geoduck clams have focused on their ecology, biological characteristics, and seed production [9,10,11,12], currently, research on geoduck clams is lacking, and no species identification of geoduck clams has been reported to date. Therefore, understanding species diversity and population density is crucial for the sustainable management of fishery resources and the conservation of important bivalve species, such as geoduck clams.
Mitochondrial genomes have been widely used as genetic markers for phylogenetic analyses and species identification [13,14]. Recently, complete animal mitochondrial genomes have also been applied to DNA barcoding-based comparative genomics, conservation biology, and evolutionary genomics [15,16]. Previous studies have reported the complete mitochondrial genome of geoduck clams, including Panopea generosa [17], Panopea globosa [18], and Panopea abrupta [3]. However, to date, there has been no report of the complete mitochondrial genome of the native geoduck clam in South Korea.
In general, for the conservation, management, and sustainable use of bivalve resources, many environmental factors (e.g., temperature, salinity, and food type) that influence the functioning of bivalve physiological processes must be considered. In particular, temperature is the main environmental factor influencing various physiological processes, including growth and reproduction in marine organisms [19,20]. Temperature influences the reproductive characteristics of marine bivalves, including clams [21,22,23,24,25]. In addition, understanding the reproductive system is essential for the mass production of commercially valuable marine bivalves. However, no information is available on the characteristics of the reproductive biology of the native geoduck clam in South Korea.
In this study, we sequenced the complete mitochondrial genome of native geoduck clam specimens collected from South Korea, providing species identification based on brief morphological information and phylogenetic classification. In addition, we investigated the sex ratio, gametogenesis, and reproductive cycle of native geoduck clams. This study provides important information for future populations and evolutionary studies associated with the conservation of native geoduck clams in South Korea.
2. Materials and Methods
2.1. Sampling Collection
Sampling for this study was conducted using a hookah diving system from Gosung’s Bongpo and Yangyang’s Ingu on the east coast of South Korea. The sampling areas are shown in Figure 1. Live geoduck clams were collected every month (20 bivalves/month) from subtidal medium sand and coarse sand (Mean ø 2.1 ± 0.4 mm) at 13.0–27.3 m depth in Gangwon province, approximately 40–60 cm deep in soft sediments, from September 2018 to August 2019. At the time of sampling, the surface (the bottom-water temperature at 30 m depth) and the surface (bottom) salinity ranged from 11.0–23.5 (8.0–16.5 °C) and 28.3–34.2 (34.0–35.9 psu), respectively (Figure 2).
2.2. DNA Extraction and Sequencing
Genomic DNA was extracted from muscle tissues using the DNeasy Blood and Tissue Kit (Qiagen, Hilden, Germany) following the manufacturer’s protocol. The quantity and quality of the extracted genomic DNA were measured using a Victor3 multilabel plate reader (PerkinElmer, Waltham, MA, USA). A genomic library was constructed using the TruSeq Nano DNA Kit by a commercial company (Macrogen, Seoul, Republic of Korea) according to the manufacturer’s instructions (Illumina, San Diego, CA, USA). The complete mitochondrial genome of Panopea sp. was assembled and annotated using MITOS [26].
2.3. Sequence Alignment and Phylogenetic Analysis
The complete mitochondrial genomes of 10 bivalve species (5 families; Arcticidae, Cardiidae, Hiatellidae, Myidae, and Lucinidae) were downloaded from the GenBank database and used to construct a phylogenetic tree (Table 1). The concatenated set of the 13 protein-coding genes (PCGs) for each mitochondrial genome was aligned using the ClustalW algorithm in MEGA software (ver. 10.0.1; Center for Evolutionary Medicine and Informatics, Tempe, AZ, USA). To establish the best-fit substitution model for phylogenetic analysis, the model with the lowest Bayesian Information Criterion and Akaike Information Criterion scores was estimated using a maximum-likelihood (ML) analysis. According to the results of the model test, ML phylogenetic analyses were performed using the LG + G + I model in the MEGA software. Support for the nodes was calculated using 1000 bootstrap replicates.
2.4. Morphological Characteristics
For the species identification of the Korean geoduck clam, a morphological analysis of the shell characters was performed. Living specimens of Panopea sp. were fixed in 95% ethanol, and their valves were dissected for observation of hinge structure and shell surface sculpture. Photographic images of Panopea sp. (Figure 3) were taken using a camera equipped with a Copy Stand system (CS-920, Nikon, Tokyo, Japan). Voucher material was deposited at the Honam National Institute of Biological Resources (HNIBR). The terminology of morphological description follows a previous study on the taxonomic revision of Panopea abbreviata [27].
2.5. Histological Analysis
Every month, 20 samples of geoduck clams were randomly selected for histological examination in the rearing tank. Shell length (right valve) and height were measured using vernier calipers (±0.1 mm), and whole-body weight was weighted to the nearest gram using a digital balance (Toledo, AB-204, error = 0.01 g). The shells were opened, the gonads were collected using scissors and a knife, and two small pieces of each gonad of clam (approximately 0.5 cm) were preserved in a Bouin’s solution (5% glacial acetic acid, 9% formaldehyde, and 0.9% picric acid) for 24 h and then stored in 70% ethanol. Gonad samples were preserved for analysis. For analysis, the gonad samples were dehydrated using an ethanol series and soaked in xylene and paraffin. The samples were then embedded in a cassette and sectioned on a microtome. The 5-µm sections were placed on a slide and then kept on a hot plate for 24 h. The sectioned sample was stained with Mayer’s hematoxylin-eosin and observed under a light microscope (BX 50, X200; Olympus, Tokyo, Japan). Gonadal development was categorized into six stages, as described in a previous study [28]. The sex ratio was estimated for the total sample and analyzed to verify the deviations from a 1:1 proportion using the chi-square test.
3. Results and Discussion
The geoduck clam specimens collected from the east coast of South Korea were assigned as members of the genus Panopea based on the following generic morphological features: the presence of one cardinal tooth in the hinge and an enlarged siphonal extension that fit into the mantle [2]. The morphological features of the Korean specimens were as follows: a thick to thin shell, subquadrate, white in color, with gaping anteriorly and posteriorly; a wider posterior gap than the anterior one; length from beak to anterior margin occupying 42% of the total shell length; an external surface with a sculpture composed of commarginal folds and weak growth lines; rounded anterior end, posterior ridge truncated to slightly produced ventrally; slightly concave ventral margin; weakly prominent umbo, subcentral anteriorly; prominent ligament, dark brown in color; thin periostracum, tan in color, dehiscent; short nymph; a hinge with a single cardinal tooth, which slightly curved towards the dorsal margin, in each valve; small anterior adductor scar, dorsally positioned; posterior adductor scar reinforms, positioned dorsally; continuous pallial line; anterior line slightly produced; and posterior line truncate. The pallial sinuses are shallow in both valves. The postvalvular extension was 710 mm long in preserved specimens (in ethanol) with fused siphons distally; a length of up to 960 mm; and a height of up to 590 mm.
In this study, we sequenced the complete mitochondrial genome of Panopea sp. The length of the complete mitochondrial genome of Panopea sp. was 16,006 bp (GenBank number: OQ469487), which is longer than those of P. abrupta (15,381 bp), P. globosa (15,469 bp), and P. generosa (15,585 bp) [3]. The complete mitochondrial genome of Panopea sp. contained 13 PCGs, 22 transfer RNAs, 2 ribosomal RNA genes, and a control region (D-loop) (Table 2 and Figure 4a). The overall base composition of the mitogenome is A 25.8%, T 38.4%, C 11.4%, and G 24.4%, which is similar but slightly different from that of P. abrupta (A 25.6%, T 38.8%, C 11.3%, and G 24.3%), P. generosa (A 25.0%, T 38.7%, C 11.2%, and G 25.0%), and P. globosa (A 23.3%, T 40.4%, C 10.1%, and G 26.1%). Additionally, species-specific differences may be attributed to differences in composition. For example, the A+T and G+C compositions of the 13 PCGs were 63.7% and 36.3% in the mitochondrial genome of Panopea sp. and 64.2% and 35.8% in all sequences, respectively. The ratio of A+T nucleotides in the mitochondrial genome of Panopea sp. was similar to that of P. abrupta (64.4%) but higher than those of congeneric species P. generosa (63.7%) and P. globosa (63.7%). In addition, in Panopea sp., the 12 PCGs initiate with the start codon ATG/GTG whereas nad4 initiates with the start codon ATA. All PCGs were terminated with TAA/TAG. In contrast to Panopea sp., 12 PCGs initiate with the start codon ATG/GTG, whereas COXIII has the start codon ATA in P. abrupta. All PCGs were terminated with TAA/TAG. Therefore, the comparative analysis of mitogenomes in Panopea sp. showed species-specific differences in the mitogenomes of Panopea species.
In this study, the molecular phylogenetic tree showed that the Panopea species collected from the east coast of South Korea were genetically distinct from each other and belonged to the genus Panopea (Figure 4b). In particular, Korean Panopea species clustered with the P. abrupta Chinese strain with a bootstrap value of 100%. A previous study reported the occurrence of P. abrupta on Chinese coasts, determined its complete mitochondrial genome sequence, and found a sister relationship between P. abrupta and P. generosa. However, the validity of the species identification is uncertain since the species name of P. abrupta was previously used for a fossil species [29]. The taxonomy and nomenclature of P. abrupta have a complex history. P. abrupta was originally introduced from the Miocene deposits of Oregon in the Northwest Pacific region of the USA; however, this species name had been erroneously considered as an extant species P. generosa occurring in the Northeastern Pacific coasts in the previous malacological literature published in 1983–2009 [29]. Based on the morphological differences between the holotypes of the two species in the anterior gap, the junior synonym of P. generosa from P. abrupta was removed. Gould’s holotype of P. generosa has a distinct anterior gap whereas it is absent in Conard’s fossils of P. abrupta. Thus, we suspect that the geoduck clam specimens collected from the coast of China might be an undescribed species of Panopea. Additionally, in our study, although the molecular phylogenetic results of the complete mitogenomes of Panopea sp. from China and South Korea showed a close relationship with P. generosa (Figure 4b), they are distinct species based on the following morphological differences: the ratio of shell height/shell length in P. generosa (0.66; Figure 5 and Figure 6) is slightly higher than that in Panopea sp. (0.61; Figure 3b,c); the anteroventral margin of the shell in P. generosa is weakly angled whereas it is smoothly rounded in our Panopea sp.; in dorsal view, the outlines of both shells in P. generosa are nearly parallel from the umbo to the posterior end (Figure 4) compared to those of our Panopea sp. (Figure 3a); and the pallial sinus of Panopea sp. is distinctly deep whereas it is weakly developed in P. generosa (Figure 3c) [29]. Taken together, our results suggest that the geoduck clam specimens collected are the first report of the genera Panopea on the east coast of South Korea.
Table 3 shows the sex ratio during the study period. Of the total 220 individuals, 77 (35.0%) were females, 137 (62.3%) were males, and 6 (2.7%) were undifferentiated. The sex ratio of the geoduck clams was skewed towards males from May 2019 to July 2019. The overall female-to-male ratio was 0.56:1, which significantly differed from 1:1 (Chi-square test, p < 0.05, df = 1). A previous study reported that the sex ratio of P. abbreviate was biased toward males with a total length of less than 90 mm [28]. Moreover, previous studies have suggested that a disparate sex ratio in P. abbreviata related to protandry occurs in the Panopea genus [28,30,31,32]. In the present study, we observed sex ratio bias in males between May 2019 and July 2019, when individuals smaller than females intensively appeared. This also appears to be due to the characteristics of the protandry mechanism of this species. However, the hermaphrodites of this species have not been detected, and the patterns of the protandry mechanism require further investigation.
The microscopic features of the process of developing gonads in male and female geoduck clams are shown in Figure 5 and Figure 6. The early active stage in males is characterized by small follicles filled with spermatogonia (Figure 5a). Oogonia were attached to the inner follicle wall, and some developing oocytes were observed in females (Figure 6a). In the late active stage, the follicles contained numerous spermatocytes, which are rounded cells that are highly eosinophilic in the male gonads (Figure 5b), and the primary oocytes increased in size and number in the follicles of the female gonads (Figure 6b). In the ripe stage in males, characterized by large, full follicles filled with spermatozoa (Figure 5c), the follicles were filled with mature oocytes in the female gonads (Figure 6c). During the spawning stage of males, the gonad follicles of the spawned males showed an empty area that contained an array of spermatozoa (Figure 5d). Additionally, the female gonad follicles showed a sparse form, indicating that the remaining oocytes were free from the follicle wall (Figure 6d). In the spent stage, the male gonads were atrophic and irregular in follicles and often formed sperm ducts filled with connective tissue (Figure 5e). In females, empty follicles surrounded by connective tissue females and residual oocytes were observed (Figure 6e). In previous studies, the gonadal development of P. ganerosa, P. abrupta, and P. abbreviata was assigned to one of six stages [28,30,32], including undifferentiated stages, which are indistinguishable from immature males and females. In the present study, the gonadal development stage was assigned according to previous studies and classified into six types with slight modifications.
The ripe and spawning stages of gonads were observed from October 2018 to April 2019 with dominant stages in both sexes when the water temperature dropped below 19.3 °C (surface) and 13.7 °C (bottom) and increased to 11.5 °C (surface) and 7.5 °C (bottom) (Figure 2 and Figure 7). Subsequently, the ripe and spawning stages were observed intermittently in both sexes with differences in gonadal development timing or asynchrony from May to August 2019. The frequency of the gonad stage indicated that the main spawning activity occurred from October to April, with no clear spawning pattern from May to August 2019 (Figure 5 and Figure 6). In previous studies, burrowing species such as Panopea abbeviata, P. japonica, Protothaca antiqua, and Ensis macha, these species have a protracted spawning season or two periods of spawning seasons [28,33,34,35,36]. Moreover, a previous study reported that P. abbreviata populations in northern Argentinean Patagonia show a protected spawning season with no clear pattern of spawning peaks and suggested that P. abbreviata live in thermal stability environments, such as burrowing species buried more than 70 cm in soft sediments, which could explain the protracted spawning period [28]. In our study, geoduck clams were sampled at more than 40 cm depth in sediments, and it seems that there was a protracted spawning season with no clear pattern of spawning peaks in thermal stability in sediments. However, the patterns of spawning ratios with the protandry mechanism have not been determined. The occurrence pattern of hermaphrodites at this site should be further investigated to understand their reproductive strategy.
In summary, we determined, for the first time, the complete mitochondrial genome of the geoduck clam specimen collected from the east coast of South Korea and conducted phylogenetic analyses within the subclass Heterodonta. In addition, we investigated the monthly changes in the sex ratio, gametogenesis, and reproductive cycle of Panopea sp. from September 2019 to August 2020 in females and males. Overall, this study provides critical information for population and conservation genetics for the management and use of clam resources.
Author Contributions
Data curation, formal analysis, writing—original draft, J.H.; investigation, J.G.K.; project administration, funding acquisition, O.-N.K.; conceptualization, formal analysis, writing—original draft, Y.-U.C. All authors have read and agreed to the published version of the manuscript.
Funding
This study was supported by the Korea Institute of Marine Science & Technology Promotion (KIMST) funded by the Ministry of Oceans and Fisheries (2018-0377) and also supported by KIOST project (PEA0122).
Institutional Review Board Statement
All experiments were conducted in compliance with the guidelines of the Institutional Animal Care and Experimental Committee of the Korea Institute of Ocean Science and Technology (KIOST) which approved the experimental protocol.
Informed Consent Statement
Not applicable.
Data Availability Statement
All data generated or analyzed during this study are available via the data repository of the KIOST. Requests for material should be made to the corresponding author.
Acknowledgments
We are thankful to the Moongeun Yoon of the National Marine Biodiversity Institute of Korea for his help and friendly attitude during our research work. Finally, we thank the editor and the anonymous reviewers whose comments greatly improved the manuscript.
Conflicts of Interest
The authors declare no conflict of interest.
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Figure 1.
Sampling sites of the Eastern Geoduck clam, Panopea sp. on the east coast of South Korea.
Figure 2.
Surface (0 m) and bottom (30 m) water temperatures (°C) of the sampling sites of Eastern Geoduck clam, Panopea sp. in South Korea.
Figure 2.
Surface (0 m) and bottom (30 m) water temperatures (°C) of the sampling sites of Eastern Geoduck clam, Panopea sp. in South Korea.
Figure 3.
Photographs of Panopea sp. examined in the present study. (a) dorsal view of the habitus; (b) lateral view of the habitus (left side); (c) interior of the left valve; and (d) hinge of the right valve.
Figure 3.
Photographs of Panopea sp. examined in the present study. (a) dorsal view of the habitus; (b) lateral view of the habitus (left side); (c) interior of the left valve; and (d) hinge of the right valve.
Figure 4.
(a) The mitochondrial genome map of geoduck clam, Panopea sp. (b) Maximum-likelihood phylogeny of the complete mitogenomes. The red triangle indicates the Panopea sp. analyzed in this study.
Figure 4.
(a) The mitochondrial genome map of geoduck clam, Panopea sp. (b) Maximum-likelihood phylogeny of the complete mitogenomes. The red triangle indicates the Panopea sp. analyzed in this study.
Figure 5.
Photomicrographs of histological sections of the geoduck clam, Panopea sp. male gonads at gametogenesis. (a) Early active; (b) Late active; (c) Ripe; (d); Spawning, and (e) Spent stages. Scale bar = 100 μm. sg, spematogonia; sd, sperm duct; ct, connective tissue; f; follicle; sc, spermatopcyte; sz, spermatozoa; ph, phagocytes.
Figure 5.
Photomicrographs of histological sections of the geoduck clam, Panopea sp. male gonads at gametogenesis. (a) Early active; (b) Late active; (c) Ripe; (d); Spawning, and (e) Spent stages. Scale bar = 100 μm. sg, spematogonia; sd, sperm duct; ct, connective tissue; f; follicle; sc, spermatopcyte; sz, spermatozoa; ph, phagocytes.
Figure 6.
Photomicrographs of histological sections of the geoduck clam, Panopea sp. female gonad sat gametogenesis. (a) Early active; (b) Late active; (c) Ripe; (d); spawning, and (e) Spent stages. Scale bar = 100 μm. oog, oogonia; ct, connective tissue; f; follicle; do, developing oocytes; mo, maturing oocytes; ph, phagocytes.
Figure 6.
Photomicrographs of histological sections of the geoduck clam, Panopea sp. female gonad sat gametogenesis. (a) Early active; (b) Late active; (c) Ripe; (d); spawning, and (e) Spent stages. Scale bar = 100 μm. oog, oogonia; ct, connective tissue; f; follicle; do, developing oocytes; mo, maturing oocytes; ph, phagocytes.
Figure 7.
Monthly variation in gonad developmental stages of geoduck clam, Panopea sp. collected from the east coast of South Korea from September 2019 to August 2020. Upper, females; lower, males.
Figure 7.
Monthly variation in gonad developmental stages of geoduck clam, Panopea sp. collected from the east coast of South Korea from September 2019 to August 2020. Upper, females; lower, males.
Table 1.
List of complete mt genomes used in this study.
| Family | Species | Size (bp) | Accession No. |
|---|---|---|---|
| Arcticidae | Arctica islandica | 18,289 | NC_022709 |
| Cardiidae | Acanthocardia tuberculata | 16,104 | NC_008452 |
| Cardiidae | Fulvia mutica | 19,110 | NC_022194 |
| Cardiidae | Tridacna squamosa | 20,930 | NC_026558 |
| Hiatellidae | Panopea abrupta | 15,381 | KX494111 |
| Hiatellidae | Panopea generosa | 15,585 | NC_025635 |
| Hiatellidae | Panopea globosa | 15,469 | NC_025636 |
| Lucinidae | Loripes lacteus | 17,321 | NC_013271 |
| Lucinidae | Lucinella divaricata | 18,940 | NC_013275 |
| Myidae | Mya arenaria | 17,947 | NC_024738 |
Table 2.
Summary of Panopea sp. mitogenome.
| Full Gene Name | Location | Size (bp) | Start Codon | Stop Codon | Intergenic Region * |
|---|---|---|---|---|---|
| Cytochrome c oxidase subunit I (cox1) | 1–1563 | 1563 | GTG | TAG | 0 |
| D-lopp (DR) | 1564–2401 | 838 | - | - | 0 |
| Cytochrome c oxidase subunit II (cox2) | 2402–3139 | 738 | ATG | TAA | 10 |
| tRNA-Val (trnV) | 3150–3214 | 65 | - | - | 2 |
| tRNA-Thr (trnT) | 3217–3282 | 66 | - | - | 69 |
| tRNA-Tyr (trnY) | 3352–3413 | 62 | - | - | 10 |
| NADH dehydrogenase subunit 4L (nad4l) | 3424–3714 | 291 | ATG | TAG | 52 |
| ATP synthase F0 subunit 8 (atp8) | 3767–3880 | 114 | ATG | TAA | 163 |
| NADH dehydrogenase subunit 4 (nad4) | 4044–5231 | 1188 | ATA | TAG | 0 |
| tRNA-His (trnH) | 5232–5295 | 64 | - | - | 0 |
| tRNA-Glu (trnE) | 5296–5359 | 64 | - | - | −5 |
| tRNA-Ser2 (trnS2) | 5355–5417 | 63 | - | - | 3 |
| NADH dehydrogenase subunit 3 (nad3) | 5421–5786 | 366 | ATG | TAG | −1 |
| tRNA-Ile (trnI) | 5786–5852 | 67 | - | - | 6 |
| tRNA-Asp (trnD) | 5859–5922 | 64 | - | - | 4 |
| tRNA-Lys (trnK) | 5927–5989 | 63 | - | - | 2 |
| tRNA-Leu2 (TrnL2) | 5992–6056 | 65 | - | - | 0 |
| NADH dehydrogenase subunit 1 (nad1) | 6057–6980 | 924 | ATG | TAG | 1 |
| tRNA-Leu1 (TrnL1) | 6982–7046 | 65 | - | - | 32 |
| tRNA-Asn (TrnN) | 7079–7146 | 68 | - | - | 1 |
| NADH dehydrogenase subunit 5 (nad5) | 7148–8872 | 1725 | ATG | TAA | −1 |
| NADH dehydrogenase subunit 6 (nad6) | 8872–9399 | 528 | ATG | TAA | −1 |
| tRNA-Arg (trnR) | 9399–9462 | 64 | - | - | 2 |
| Cytochrome b (cob) | 9465–10,618 | 1154 | GTG | TAA | 13 |
| tRNA-Trp (trnW) | 10,632–10,698 | 67 | - | - | 0 |
| 16S ribosomal RNA (trnL) | 10,699–11,931 | 1233 | - | - | 0 |
| ATP synthase F0 subunit 6 (atp6) | 11,932–12,639 | 708 | ATG | TAA | 7 |
| tRNA-Met (trnM) | 12,647–12,710 | 64 | - | - | 1 |
| 12S ribosomal RNA (rrnS) | 12,712–13,574 | 863 | - | - | 0 |
| Cytochrome c oxidase subunit III (cox3) | 13,575–14,360 | 786 | ATG | TAG | 4 |
| tRNA-Ser1 (trnS1) | 14,365–14,431 | 67 | - | - | 0 |
| NADH dehydrogenase subunit 2 (nad2) | 14,432–15,478 | 1047 | ATG | TAA | 13 |
| tRNA-Gln (trnQ) | 15,492–15,557 | 66 | - | - | 8 |
| tRNA-Phe (trnF) | 15,566–15,628 | 63 | - | - | 14 |
| tRNA-Cys (trnC) | 15,643–15,707 | 65 | - | - | 22 |
| tRNA-Pro (trnP) | 15,730–15,796 | 67 | - | - | 10 |
| tRNA-Gly (trnG) | 15,807–15,872 | 66 | - | - | 15 |
| tRNA-Ala (trnA) | 15,888–15,952 | 65 | - | - | - |
* Negative numbers indicate overlapping nucleotides between adjacent genes.
Table 3.
Number and size ranges of females and males, and sex ratios for each monthly sample (undifferentiated individuals are omitted).
Table 3.
Number and size ranges of females and males, and sex ratios for each monthly sample (undifferentiated individuals are omitted).
| Month | Sex Categories | Sex Ratio | |
|---|---|---|---|
| Female | Male | ||
| September | 8 (85.9–111.3) | 9 (91.7–113.8) | 0.88:1 |
| October | 12 (101.5–127.0) | 8 (103.5–129.0) | 1.50:1 |
| November | 6 (82.4–120.7) | 14 (80.5–129.0) | 0.42:1 |
| January | 9 (104.0–117.2) | 10 (101.5–134.4) | 1:1 |
| February | nd | nd | nd |
| March | 11 (80.5–130.5) | 9 (80.5–128.5) | 1.22:1 |
| April | 8 (80.5–125.1) | 12 (82.4–127.0) | 0.66:1 |
| May | 2 (109.4–117.2) | 18 (82.4–122.6) | 0.11:1 * |
| June | 3 (105.5–125.1) | 17 (78.5–112.8) | 0.17:1 * |
| July | 2 (103.3–118.2) | 17 (74.6–115.5) | 0.11:1 * |
| August | 6 (81.6–135.9) | 13 (86.3–112.8) | 0.46:1 |
| Total | 77 | 137 | 0.56:1 * |
*, differs significantly from 1:1 (Chi-square test, p < 0.05, df = 1); nd, no data available.
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MDPI and ACS Style
Han, J.; Kim, J.G.; Kwon, O.-N.; Choi, Y.-U. New Record of Geoduck Clam Collected from the East Coast of South Korea and Its Reproductive Characteristics. J. Mar. Sci. Eng. 2023, 11, 776. https://doi.org/10.3390/jmse11040776
AMA Style
Han J, Kim JG, Kwon O-N, Choi Y-U. New Record of Geoduck Clam Collected from the East Coast of South Korea and Its Reproductive Characteristics. Journal of Marine Science and Engineering. 2023; 11(4):776. https://doi.org/10.3390/jmse11040776
Chicago/Turabian StyleHan, Jeonghoon, Jong Guk Kim, O-Nam Kwon, and Young-Ung Choi. 2023. "New Record of Geoduck Clam Collected from the East Coast of South Korea and Its Reproductive Characteristics" Journal of Marine Science and Engineering 11, no. 4: 776. https://doi.org/10.3390/jmse11040776
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