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Information about the reproductive cycles of commercially important species is most fundamental in fishery management and culture development. Reproductive cycles of marine bivalves distributed in temperate coastal waters are affected not only by endogenous factors but also by seasonally changing environmental factors, such as water temperature, salinity, and food availability (Eversole 2001, Gosling 2015), which is a cause of differences in their reproductive cycles among populations in several spatial scales (Newell et al. 1982, Borrero 1987, Santos et al. 2011, Hernandez-Otero et al. 2014). A mismatch between the timing of spawning and optimal environmental conditions for larval development results in reduced larval growth rates and may elevate risks of predation and larval transport to offshore unsuitable areas due to the prolonged pelagic larval duration; and hence, among the aforementioned environmental factors, for bivalves with a lecithotrophic planktonic larval phase in their early life stages, water temperature might be the major limiting factor for their larval growth and consequently more influential on the timing of spawning (Philippart et al. 2014).

The razor clam Solen gordonis (Yokoyama, 1920) is a suspensionfeeding infaunal bivalve with a maximum shell length (SL) of 110 mm, inhabiting sandy bottoms (5- to 20-m water depths) along the coastlines of western Japan, South Korea, and Taiwan (Kawahara & Minagawa 1970, Chung et al. 1986, Matsukuma 2000, Takeuchi et al. 2016). In some Japanese coastal waters (e.g., Seto Inland Sea, Sasebo Bay; Fig. 1), they are commercially harvested from boats, using bundles of ca. 1-m-long metal rods each with a cone-shaped tip to pierce S. gordonis clams vertically (Kawahara & Minagawa 1970, Takeuchi et al. 2016). In Sasebo Bay, harvesting for S. gordonis clams is mainly conducted during early January to late April. The fishery has clam-size selectivity in which larger clams are pierced more firmly by the fishing gear than smaller clams (mean SLs for catches and noncatches are 74.3 and 69.7 mm, respectively), and consequently, most of the latter clams are detached from the fishing gear and left on the seafloor (Takeuchi et al. 2016). As a result, a considerable noncatch mortality being roughly equal to fishing mortality arises. Nevertheless, a municipal project of Sasebo City aiming to improve harvesting and to commercially brand S. gordonis clams harvested from Sasebo Bay has been in progress since 2012 (Takeuchi et al. 2016). Despite the increasing commercial demand and fishery impact on the population, information about its ecology remains limited (Takeuchi et al. 2016).

The reproductive cycle of the Solen gordonis population in Sasebo Bay remains unclear. A study on the reproductive cycle of this species using histological analysis has been conducted only for a population in the coastal area of Dadaepo, Pusan, South Korea (Chung et al. 1986). The previous study reported that spawning occurred once a year during May to June, a period of increasing water temperature. By contrast, spawning of the S. gordonis population in Sasebo Bay appears to take place once a year for the period during October to November, a period with a decreasing water temperature, as suspected from the following three items: (1) a remarkable decline in a body condition index of the population from October to November; (2) the presence of well-developed gonads enough to be observed macroscopically, in all specimens collected in October; and (3) the occurrence of new recruits with a mean SL of 4 mm in November (Takeuchi et al. 2016). There is, however, no evidence supporting this estimation from a histological perspective. In a larval rearing experiment for S. gordonis in a no-food condition at approximately 20[degrees]C water temperature, planktonic larvae, which were hatched out from fertilized eggs (ca. 90-100 [micro]m in diameter) produced by brood stocks from Sasebo Bay, developed into postlarval stage after at least 7 days of culture (T. Tanigawa, unpublished data). The fact implies that they are lecithotrophic planktonic larvae, and thus the relationship between their reproductive cycle and water temperature is focused on in this article.

The primary objective of the present study was to reveal the reproductive cycle of the Solen gordonis population in Sasebo Bay, by using histological analysis. For this purpose, clams were collected from the bay at almost monthly intervals over a year by a fishing boat using a gear for the fishery or by scuba-equipped divers, and two abiotic parameters (i.e., water temperature and salinity) were monitored at the sampling locations. The present study also provided the first opportunity to report a gonadal infection by trematode and Marteilia-like parasites in S. gordonis clams.


Study Area

Sasebo Bay is located in northwestern Kyushu, Japan (33[degrees]7' N, 129[degrees]43' E; Fig. 1). The whole area covers ca. 43 [km.sup.2] and has a mean water depth of 14 m. The tide of this bay varies with a semidiurnal cycle, and mean tidal ranges are 2.5 m at spring tide and 1.0 m at neap tide. Sasebo Bay connects westward with the East China Sea and southeastward with Omura Bay via the Hario Straits (ca. 200 m in width) and the Haiki Channel (20 m in width). Water exchange between the two bays occurs mostly via the Hario Straits (Kikukawa et al. 2002). Fishing grounds for Solen gordonis clams in Sasebo Bay are mainly located in the southern part of this bay, where the present study was conducted (5- to 20-m water depths; black-filled area in Fig. 1B). There are some differences in sediment characteristics between the fishing grounds and adjacent nonfishing areas (i.e., coarse sand with shell fragments versus fine sand), but no differences in seawater conditions (for details, see Takeuchi et al. 2016).

Clam Collecting and Subsequent Procedures

In the present study area, collection of razor clams (>50 mm in SL) for histological analysis was conducted by a fishing boat using a gear for the fishery or by scuba-equipped divers on February 17, 2016, March 17, April 16, May 16, July 26, September 12, October 7, November 9, and December 7. All these dates were at around neap tides. On each sampling date, 26-56 clams were collected (306 individuals in total). The clams were fixed with 25% (but 10% on the first four dates) neutralized seawater formalin. Eventually, 8% of the clams were not used in the subsequent analysis because of foot breakage (i.e., 281 clams were selected for histological analysis). For each specimen, SL, shell height (SH), and shell width (SW) were measured to the nearest 0.01 mm using a digimatic caliper, and wet soft tissue (STW) was weighed to the nearest 0.0001 g using an electronic balance (ENTRIS224i-1S, Sartorius). The body condition index was also calculated using the following equation (modified from Toba & Miyama 1991):

Body condition index = [[STW x 10,000]/[SL x SH x SW]],

where STW, SL, SH, and SW are the weight of wet soft tissue (g), and shell length, height, and width (mm), respectively.

Abiotic Environmental Conditions

Concurrent with the clam collection, the water temperature and salinity of bottom seawater were measured to the nearest 0.01[degrees]C and 0.01 in practical salinity unit (hereafter, omitted), respectively, by using a data logger for temperature and salinity measurements (Compact-CT, JFE Advantech) on each sampling date. A data logger for water-pressure measurements (Compact-TD, JFE Advantech) was also used to detect the vertical position of the former logger in a water column. The two loggers were attached to a rope with a sinker (3.7 kg in weight), and the sensor positions of the loggers were arranged at 0.6 m from the bottom of the sinker. The instrument was lowered from the fishing boat to the seabed vertically, recording water temperature, salinity, and water depth every second. The water temperature and salinity of seawater at 0.6 m above the seabed were extracted from the data and used in the subsequent analysis.

Histological Study

For histological analysis, 281 clams were used (25-51 clams on each sampling date). The mean SL ([+ or -]SD) of the clams was 75.5 [+ or -] 9.3 mm (range: 52.9-109.0 mm). The gonadal tissue of each specimen was processed using conventional histological methods. Gonads of Solen gordonis clams are irregularly arranged from the subregion of midintestinal gland in the visceral cavity to the reticular connective tissue of a foot (Chung et al. 1986, Takeuchi et al. 2016). For each specimen, this body part was transversally excised into three 5-mm-thick sections spaced 5 mm apart from each other. The excised sections including gonadal tissue were dehydrated in a series of ethyl alcohol solutions, cleared in methyl benzoate, embedded into paraffin, sliced to 3-[micro]m-thick sections using a rotary microtome (HM 325, MICROM). and stained with hematoxylin and eosin. The sex and reproductive stage of each specimen were examined under an optical microscope (Axio Scope. A1, Carl Zeiss; x 200-x400). Sex was determined on the basis of the presence of spermatozoa or oocytes, and whether the sex ratio of the population differed significantly from 1:1 was tested using a chi-square test. Reproductive stage was determined in accordance with the definitions by Ayache et al. (2016) in which the reproductive cycle of the razor clam S. marginatus in the southern Mediterranean Sea was classified into the following five stages: resting (stage 0); gametogenesis (stage I); ripe (stage II); spawning (stage III); and exhaustion (stage IV). The reproductive stage of a specimen in which multiple different stages co-occurred was determined as the most abundant one among them. The proportional frequency of each reproductive stage was calculated on each sampling date. The difference in body condition index among the reproductive stages was tested using the Kruskal--Wallis test, followed by the Steel--Dwass multiple-comparison test. All statistical analyses were performed on the "R"-based software "EZR" (Kanda 2013).


Abiotic Environmental Conditions

Seasonal changes in water temperature and salinity of bottom seawater during the present study period showed a typical trend in Sasebo Bay (Fig. 2; and also see fig. 3 in Takeuchi et al. 2016). That is, water temperature and salinity varied from 11.2[degrees]C (February) to 26.1[degrees]C (September) and from 31.3 (July) to 34.0 (April), respectively.

Reproductive Stages

The reproductive stages of Solen gordonis clams were largely divided into the following five stages: resting (stage 0); gametogenesis (stage I); ripe (stage II); spawning (stage III); and exhaustion (stage IV). The detailed description for each stage is as follows:

1. Stage 0: sexually nonactive (resting) stage preceding gametogenesis. In this stage, specimens had very thin layers of follicular tissue covering the inner muscle of a foot and visceral mass, and no gametes occurred in most of the follicles (Fig. 3A). Sexes of specimens in this stage were undetermined because of lack of gametes in the histological sections, with the exception of a case where a few residual gametes were possessed (i.e., 17% of the total for this stage).

2. Stage I: gametogenesis stage. Specimens had spermatocytes and a few spermatozoa for male and oocytes for female in their follicles (Fig. 3B, F). The mean cross-sectional area ([+ or -]SD, N: number of oocytes) of oocytes with a nucleolus in photomicrographs and diameter approximated from them were 2,192.1 ([+ or -]1,310.3, N= 61) [micro][m.sup.2] and 53 [micro]m, respectively [these measurements were obtained from photomicrographs using ImageJ 1.48v (available at].

3. Stage II: ripe stage. Specimens had follicles filled with radially arranged spermatozoa for male and mature oocytes for female (Fig. 3C, G). The space of visceral cavity was fully filled by well-developed gonads. The mean cross-sectional area of oocytes with a nucleolus in photomicrographs and diameter approximated from them were 6,651.4 ([+ or -]1,509.6, N = 34) [micro][m.sup.2] and 92 [micro]m, respectively.

4. Stage III: spawning stage. Specimens had follicles possessing spermatozoa for male and oocytes for female, with some spaces associated with partial spawning (Fig. 3D, H).

5. Stage IV: sexually nonactive (exhaustion) stage after mass spawning. Follicles shrunk and were mostly empty as a result of spawning, and in some of them, a few residual gametes remained (Fig. 3E, I).

Reproductive Cycle

The spawning season of the Solen gordonis population in Sasebo Bay was in the fall season during the present study period (Fig. 4, upper panel), and their reproductive cycle was well synchronized between sexes (Fig. 4, lower two panels). For example, all specimens during February to July 2016 were in the sexually nonactive stage (i.e., stages 0 and IV); most specimens in September (=84% of total) had started gametogenesis, and after a month, most of them (=61 % of total) had developed into the ripe stage (stage II); and spawning took place for a short duration of time, during October to December, peaking in November.

Sex Ratio

Of the 281 specimens for the histological study, 28.5% and 38.1% were male and female, respectively, and the sex of the others was indistinguishable because of the reason mentioned previously. No hermaphrodite specimens were found in the present study. The ratio of male to female on each sampling date varied from 0.07 (April) to 1.67 (December) (for details, see Table 1). This ratio also differed among reproductive stages (i.e., 0.46 in stage 0, 0.76 in stage I, 1.21 in stage II, 1.13 in stage III, and 0.60 in stage IV). To correct the bias in the sex ratio due to the inclusion of specimens in stage 0, they were not used in a test for sex ratio biasing. Eventually, the ratio of male to female was corrected as 0.82 (i.e., 45.1% and 54.9% of the 162 specimens in stages I-IV were male and female, respectively). The result of a chi-square test on the corrected sex ratio data showed no significant deviation from 1:1 (P = 0.21).

Body Condition Index

Temporal variation in the mean body condition index of specimens on each sampling date was found, being largely divided into three temporal phases [i.e., from February to April (middle-level phase), from May to October (high-level phase), and from November to December (low-level phase); Fig. 5A]. The mean value ([+ or -]SD, N: number of specimens) for each phase was 4.79 ([+ or -]0.38, N = 86); 5.30 ([+ or -]0.63, N = 138); and 3.76 ([+ or -]0.44, N = 57), respectively. Body condition index also varied significantly among reproductive stages (P < 0.001, Kruskal--Wallis test; Fig. 5B). The median (first--third quartiles) of the body condition index for each reproductive stage was 5.03 (4.61-5.46) for stage 0; 5.42 (5.08-5.53) for stage I; 5.45 (5.015.66) for stage II; 3.84 (3.68-4.30) for stage III; and 4.74 (4.045.03) for stage IV. The Steel--Dwass multiple-comparison test detected significant differences between stage III and any of stages 0-II (P < 0.001); stage IV and any of stages 0-II (P < 0.001 or 0.001 < P < 0.01); and stages III and IV (0.001 < P < 0.01).

Gonadal Infection by Trematode and Marteilia-like Parasites

In some specimens for the present histological study, gonadal infection by trematode (sporocysts and cercariae) and Marteilia-like parasites was observed (Fig. 6). The infections observed in the photomicrographic images (Fig. 6A' for trematode parasites; Fig. 6B' for Marteilia-like parasites) had similar morphological characteristics of parasitic infections previously reported for other species of the superfamily Solenoidea (Lopez & Darriba 2006, Lopez-Flores et al. 2008, Orellana & Lohrmann 2015, Ruiz et al. 2016). The reproductive stages of some reproductive clams (i.e., six clams of total) were undetermined because of lack of gametes in the histological sections, associated with the high infection intensity. Gonadal infection by trematode parasites was found in specimens of both sexes during July to November 2016 (Fig. 6A). The prevalence rate of trematodes on each sampling date ranged from 0% (February to May and December) to 13.3% (November). The mean SLs ([+ or -]SD, N: number of specimens) of infected and noninfected clams were 70.1 ([+ or -]7.4, N = 11) mm and 72.7 ([+ or -]9.7, N = 124) mm, respectively (figure not shown). To determine any size preference in the infection, a generalized linear model assuming a binomial error distribution and a logit-link function was fitted to a data set that consisted of binary data (1 and 0 for infected and noninfected clams, respectively) as the response variable (y) and SL (mm) as the explanatory variable (x), and the significance of the explanatory variable was assessed using a null model likelihood ratio test; all statistical analyses were performed using "R" (R Core Team 2015). Consequently, no significance of the explanatory variable was detected (P = 0.38). On the other hand, gonadal infection by Marteilia-like parasites was found only in female specimens during September to December 2016 (Fig. 6B). The prevalence rate of Marteilia-like parasites on each sampling date ranged from 0% (February to July) to 23.3% (November). The mean SLs ([+ or -]SD, N) of infected and noninfected clams were 81.0 ([+ or -]9.7, N = 20) mm and 76.0 ([+ or -]10.6, N = 113) mm, respectively (figure not shown). The results of generalized linear model analysis with a null model likelihood ratio test detected a weak statistical significance of the explanatory variable which positively influences the response variable (P = 0.05). The obtained linear predictor was expressed as follows: y = -5.320 + 0.046x.


It is thought that a mass-spawning event of the Solen gordonis population in Sasebo Bay occurs once a year for a short time duration, during October to November (Takeuchi et al. 2016). This estimation was strongly supported by the present results from a histological perspective. For example, the reproductive cycle of the S. gordonis population in Sasebo Bay showed a reproductive resting for a long time duration during February to July, gametogenesis sharply advanced in September, and spawning took place over a short period, during October to December, with a peak in November (Fig. 4). This cycle was well synchronized between sexes. By contrast, Chung et al. (1986) report that spawning of a S. gordonis population in South Korea occurs once a year during May to June. Gametogenesis of the population in Sasebo Bay was initiated at approximately 25[degrees]C water temperature (Fig. 2), whereas that of the population in South Korea was initiated at approximately 10[degrees]C (Chung et al. 1986). Such a difference between the two S. gordonis populations would suggest that water temperature was not important to initiate gametogenesis for this species. On the other hand, it was well consistent between the two S. gordonis populations that spawning occurs at approximately 20[degrees]C water temperature. Spawning of other Solen species distributed around the geographical regions also occurs at approximately 20[degrees]C water temperature (for a Solen strictus population in Japan, see Kawahara & Kato 1971; for a S. strictus population in South Korea, see Chung et al. 1986; and for a S. grandis population in South Korea, see Chung & Park 1998). This species (S. gordonis) has a lecithotrophic development phase in its early life stages (T. Tanigawa, unpublished data). Given the fact, the timing of their spawning might be focused on water temperature which is suitable for their larval development and survival, as stated for the oyster Crassostrea gigas (Philippart et al. 2014). To examine whether this supposition is true, a future study comparing larval development and survival among a variety of water temperatures is required.

The sex ratio of the Solen gordonis population in Sasebo Bay was 1:1. The ratio, however, varied with time (Table 1). For example, in the mid sexually nonactive period (i.e., April to May), the ratio biased to females was observed. Some delay in the period of stage IV was also observed in females compared with males (Fig. 4). For example, in the mid sexually nonactive period, the mean proportional frequency of stage IV was 16.7% for males, whereas 53.2% for females. The efficiencies of gamete emission and/or resorption for oocytes might be lower than those for spermatozoa, and such differences between sexes could lead to temporal variation in sex ratio.

Immediately after the spawning, the body condition index of the Solen gordonis clams from Sasebo Bay remarkably declined (Fig. 5A). A similar tendency was previously observed in the population (Takeuchi et al. 2016). Body condition index also differed significantly among the reproductive stages (P < 0.001, Kruskal--Wallis test). The value was lowest in stage III (i.e., spawning stage), followed by stage IV (exhaustion stage) and the other stages (resting--ripe stages) in order (Fig. 5B). The value of specimens in stage II was ca. 1.5 times higher than that in stage III. These findings indicate that the body condition index is also a useful quantitative scale to detect the timing of spawning but not to detect gametogenesis. As with other species of the superfamily Solenoidea, it would be appropriate to use the gonadal condition index instead of the body condition index as a quantitative scale for the reproductive cycle of the S. gordonis population (Darriba et al. 2005, Saeedi et al. 2009, Rinyod & Rahim 2011, Ayache et al. 2016).

Lowered body condition associated with its mass spawning might lead to an enhanced fishing efficiency (i.e., catch per unit effort) of the fishery for the Solen gordonis population in Sasebo Bay. For example, the fishing efficiency rises after the spawning season, with water temperatures <15[degrees]C (fig. 8B in Takeuchi et al. 2016). Even though razor clams of the superfamily Solenoidea can burrow deeply and rapidly into the sediments, compared with some other infaunal bivalve species (Trueman 1967, Stanley 1970), burrowing performance of some infaunal bivalves distributed in temperate coastal waters generally declines with decreasing water temperature (Sakurai et al. 1996, Selin 1999). In addition to this, lowered body condition makes infaunal bivalves closer to the sediment surface and slower (Zwarts & Wanink 1991, Calvez & Guillou 1998, Keino et al. 2005, Takeuchi et al. 2015). Similar to those results, S. gordonis clams in Sasebo Bay could be more easily caught by the fishing gear to pierce clams (see fig. 2 in Takeuchi et al. 2016) after the spawning season.

This is the first report of gonadal infection by trematode and Marteilia-like parasites in Solen gordonis clams. The presence of the same parasitic taxa has already been reported for other species of the superfamily Solenoidea (for Ensis macha with trematode parasites, see Orellana & Lohrmann 2015; for Solen marginatus with Marteilia sp., see Lopez & Darriba 2006; for S. marginatus with Marteilia refringens, see Lopez-Flores et al. 2008; and for S. marginatus with Marteilia octospora, see Ruiz et al. 2016). The present results also provide a little information on the clam-size preference in gonadal infection by Marteilia-like parasites. For example, their prevalence rate increased with clam size in terms of SL (for details, see the Results); and in accordance with the relationship, the prevalence rate of clams with 100-mm SL is seven times higher than the prevalence rate for 50-mm SL (i.e., 32.1% versus 4.6%). A similar tendency is found in some other filter-feeding molluscs (Leung & Poulin 2008, Gilardoni et al. 2012, and also see Taskinen & Valtonen 1995), and it is thought that older conspecifics have been exposed to parasitic infection for a longer period than younger ones and that higher filtration rate of larger conspecifics facilitates their own contact with parasite propagules in the water column. Knowledge about clam-size-dependent gonadal infection would be important to understand the host--parasite dynamics. After all, no mass mortality of the S. gordonis population by those parasites appeared to occur during the present study period (for a typical case of a collapse of a shellfishery induced by Marteilia parasites, see Villalba et al. 2014), although total reproductive output of the S. gordonis population could be somewhat limited by these parasites.

In conclusion, the present study revealed the reproductive cycle of the Solen gordonis population in Sasebo Bay and confirmed that spawning season closure for the population had already been achieved by the present harvesting schedule. For example, the spawning of the S. gordonis population in Sasebo Bay occurred during October to December, whereas the harvesting of the population is conducted during early January to late April. Gonadal infection by trematode and Marteilia-like parasites in S. gordonis was also observed for the first time. Future studies to identify the parasite species and to quantitatively assess the effects of those parasites on the S. gordonis population in Sasebo Bay are required.


We would like to thank G. Murakami and H. Harada for operating the fishing boats during the sampling, and M. Hyodo and D. Sato of Kiyo diving Co., Ltd. (Nagasaki, Japan) for conducting the clam collection. We also would like to thank T. Tanigawa for providing valuable information on Solen gordonis larvae, the staff of Hario Fisheries Cooperative Association for providing helpful comments, K. Kanai for providing a place and equipment for the laboratory work, and R. Ebisu, G. Sagara, and S. Sueki for assistance with field and laboratory works. This study was conducted as a part of the municipal project of Sasebo City to brand S. gordonis clams and partly supported by the Japan Society for the Promotion of Science Grant-in-Aid for Young Scientists (B) 17K15303 to ST.


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(1) Graduate School of Fisheries and Environmental Sciences, Nagasaki University, Bunkyo-machi 1-14, Nagasaki, Nagasaki 852-8521, Japan; (2) Faculty of Fisheries, Nagasaki University, Bunkyo-machi 1-14, Nagasaki, Nagasaki 852-8521, Japan; (3) Sasebo Municipal Fisheries Division, Hachiman-cho 1-10, Sasebo, Nagasaki 857-8585, Japan

(*) Corresponding author. E-mail:

DOI: 10.2983/035.036.0305
TABLE 1. Number of specimens of each sex and the ratio of males to
females on each sampling date. Sex of some specimens was undetermined
because of having no gametes (the fourth column).

                      Number of specimens

Date in        Male   Female   Undetermined  Total  Ratio of
2016                           sex                  males to females

February 17     9     10       13             32    0.90
March 17        7     11        8             26    0.64
April 16        1     14       13             28    0.07
May 16          3     11       19             33    0.27
July 26         0      0       29             29    -
September 12   10     11        4             25    0.91
October 7      25     22        4             51    1.14
November 9     10     19        1             30    0.53
December 7     15      9        3             27    1.67

A case with no solution is expressed as "-" in the sixth column.
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Article Details
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Author:Takeuchi, Seiji; Ishii, Yuji; Yoshikoshi, Kazuma; Takamasu, Takeshi; Nagae, Saki; Tamaki, Akio
Publication:Journal of Shellfish Research
Article Type:Report
Geographic Code:9JAPA
Date:Dec 1, 2017

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