Shell Growth and Age Determination of the Brackish Water Bivalve Corbicula Japonica in Lake Shinji, Japan

Blackwell Science, LtdOxford, UK FISFisheries Science0919-92682004 Blackwell Science Asia Pty Ltd 704August 2004 847 Growth and age of Corbicula japonica K Oshima et al. 10.1111/j.1444-2906.2004.00847.x Original Article601610BEES SGML

FISHERIES SCIENCE 2004; 70: 601–610

Shell growth and age determination of the brackish water bivalve Corbicula japonica in Lake Shinji, Japan

Kazuhiro OSHIMA,1* Naoki SUZUKI,1 Mikio NAKAMURA2 AND Kazumi SAKURAMOTO1

1Department of Ocean Sciences, Tokyo University of Marine Science and Technology, Minato, Tokyo 108-8477 and 2Japan Corbicula Research Institute, Tamayu, Shimane 699-0204, Japan

ABSTRACT: Shell growth and age determination of Corbicula japonica were investigated from samples collected monthly at two sites and field growth experiments from November 1999 to Novem- ber 2000 in Lake Shinji. Both specimens did not grow in winter when the water temperature was below 11∞C, but grew rapidly from spring to early summer when the water temperature rose from 15∞C to 30∞C, before further growing slowly from summer to autumn after the main breeding period. The monthly marginal growth distribution of the samples indicated that the concentric groove on the shell surface was an annual growth ring. It is concluded that the age of C. japonica in the i-ring group when the shell growth resumed in spring was i + 0.5 (i = 1, 2, á á ·), because the first true growth ring was formed at 0Ð2 mm in shell length, which then faded with growth. Lee’s phenomenon was observed in the age determination results, and thus the growth coefficient and the asymptotic shell length of the von Bertalanffy growth equation were not estimated from the samples. However, these parameters were estimated from the annual shell length increments of the experimental individuals, which were 0.331/year and 28.2 mm, respectively.

KEY WORDS: age determination, concentric groove, Corbicula japonica, Lake Shinji, shell growth, shell length.

INTRODUCTION morning; three types of protected areas are enforced, which are protected areas only during The bivalve Corbicula japonica is an important the summer, the annual protected areas and the species for inland fisheries in Japan. Corbicula permanently protected areas; the size of the clam japonica inhabits brackish lakes and estuaries dredge must be smaller than 60 cm in length and from Hokkaido to Kyusyu in Japan and is the dom- width, and 35 cm in height; the openings between inant species of benthic organisms in Lake Shinji, the flat bars of the clam dredge must be larger than which is located in the south-west of the mainland 11 mm. However, these regulations were not (Fig. 1). Fisheries for the C. japonica population in wholly determined in consideration of the ecologic Lake Shinji yield the maximum landing in Japan, characteristics of the species due to a lack of which is approximately 8000 t on average from knowledge. The fishery resource management 1991 to 2000. The landing in weight of the fisheries must be conducted on the basis of ecologic char- accounts for more than 90% of total landings in acteristics in order to establish the sustainable and this lake and its annual value of product was esti- effective exploitation of the population. mated to be approximately 3 billion yen from 1993 The Shimane Prefectural Freshwater Fisheries to 1998. The C. japonica population in Lake Shinji Experimental Station assessed the population size is harvested by dredge fishing. The fisheries, for of C. japonica in Lake Shinji 1–3 times a year from which the fishing rights are permitted for approxi- 1997 to 2001.1 However, the population dynamics mately 300 fishermen, is operated 4 days a week of the species has not been studied up to present. throughout the year. At present, the fisheries regu- Information on the age and growth of the target lations are as follows: the individual quota is 140 kg population is essential for fishery management. per day; the operation is permitted for 3 h in the The growth ring on the shell surface has been used for age determination in bivalves because it is con- 2–8 *Corresponding author: Tel: 81-3-5463-0565. sidered to be formed once a year. The growth of Fax: 81-3-5463-0565. Email: [email protected] C. japonica has been evaluated and age deter- Received 11 November 2003. Accepted 29 March 2004. mined by using the growth ring on the shell 602 FISHERIES SCIENCE K Oshima et al.

autumn and six times per site in winter when fewer 133°00E N 0 10 km numbers of C. japonica were gathered, because the Lake Shinji inhabitation depth of the species in the sediment was shallow during the summer and deep in win- Lake Shinji ter.14 The sediments gathered by the sampler were sorted with a sieve of 0.5-mm square mesh. Resi- Japan 35°26N dues on the sieve were ﬁxed with 10% neutral formalin. In the laboratory, the ﬁxed residues N were sieved through 4-, 1- and 0.5-mm mesh sizes. The samples of C. japonica remaining on the 4- and 1-mm-mesh sieves were sorted by eye or under a stereoscopic microscope. Juveniles of Lake Shinji C. japonica remaining on the 0.5-mm-mesh sieve were separated from the sediments under the Matsue stereoscopic microscope from November 1999 to Torigasaki January 2000. However, this procedure was time- consuming and required a great deal of attention.

Kimachi 0 5 km Sellmer described a method of small bivalve separation from sediments, using the specific gravity Fig. 1 Location of Lake Shinji. () Sampling sites; () difference between clams and sand in a concen- 15 experiment site. trated zinc chloride solution. This solution is, however, toxic and the disposal of the solution is costly. Hence, in the present study the juveniles surface9–11 or the growth line from acetate peel rep- were separated from the sediments on a 0.5-mm- licas of shell sections,12 or by size frequency.13 mesh sieve by the following procedure. Takada et al. considered the growth of C. japonica The sediments were stained with 10% neutral in Lake Shinji after age determination from liver- formalin containing sufficient quantities of rose or burnt umber-colored rings on the shell surface, bengal to distinguish the juveniles from sand and but did not clarify the relationship of the ring num- were dehydrated for 2–3 days in a drying machine ber on the shell surface to age.9 In contrast, where the temperature was kept at 60∞C, before Kawashima et al. and Utoh determined the age of being placed in a stainless steel tray full of water. C. japonica from concentric grooves on the shell The clams that rose to the surface were collected surface.10,11 The latter author confirmed that the with a dropping pipet. The bottom materials were formation of the groove was synchronized with gently stirred with a spoon to remove the clams that of the translucent layer in the shell section. from the sand particles. This procedure was The chromatic growth ring is often unrecognized repeated several times until clams were not found in aged clams or specimens with a wholly black- at the surface. The collected clams were placed in colored shell surface. Consequently, the purpose of the fixative solution and allowed to settle. The shell the present study was to investigate the growth length of 73 juveniles, which were dehydrated and characteristics of C. japonica in Lake Shinji, the had settled, were compared to those before dehy- availability of the concentric groove on the shell dration, using samples collected at Matsue in surface for age determination and the relationship February 2000. The mean shell lengths (±SD) of of the ring number on the shell surface with age. specimens before and after dehydration were 0.93 ± 0.22 mm and 0.93 ± 0.23 mm, respectively. There was no significant difference in the mean MATERIALS AND METHODS shell lengths between specimens at the 5% significance level. Consequently, dehydrating small Sampling and measurement clams did not affect their shell lengths. This method was employed for the samples obtained Samples of C. japonica were collected at Matsue from February to November 2000 in order to sepa- and Kimachi in Lake Shinji (Fig. 1), where the fish- rate small clams from sediments. ery for C. japonica is operated, once a month from The shell length (mm) of the samples collected 1 November 1999 to 2 November 2000. The sam- in the procedures described here was measured to pling gear used in the present study was a small- the nearest 0.1 mm. A sliding caliper was used to sized Smith–McIntyre grab sampler, which covered measure shell lengths larger than 3 mm, while the a surface area of 0.05 m2. Sediments were grabbed others were measured under a stereoscopic micro- by the sampler four times per site from spring to scope. The sample number of each shell length Growth and age of Corbicula japonica FISHERIES SCIENCE 603

class at 1-mm intervals were converted into the the shell surface of each individual in the MG with number of individuals per 1 m2 according to the a router in order to identify the 103 individuals. The number of grabbing times in each month, and shell four shell length classes were denoted as MG1, length distributions were estimated for samples MG2, MG3 and MG4 in ascending order, respec- collected over 13 months. tively. Table 1 shows the shell length range and the number of individuals in each MG class. The individuals of the MG group were placed in Age determination a cage (33 ¥ 57 ¥ 10 cm) of which the mesh sizes were 6 mm and 3 mm on the upper and lower Subsamples of 14–206 individuals were selected faces, respectively. The cage was placed on the from the samples obtained in Matsue from Novem- shallow bottom of the lake (approximately 70 cm ber 1999 to November 2000 for age determination. depth) at Torigasaki on 6 November 1999. The shell The periostracum of the left shell was exfoliated length (mm) and body weight (g) were individually with a 10% sodium hydroxide solution to make the measured once a month during the experimental concentric groove (termed ‘ring’) on the shell sur- period. The growth coefﬁcient k (per year) and the face easily observable. The ring number and the asymptotic shell length SL• (mm) of the von Berta- shell length at each ring were counted and mea- lanffy growth equation were estimated from the sured using the right shell. The marginal growth annual shell length increment (mm) of each indi- (mm) was deﬁned as the shell increment from the vidual in the MG. If the jth individual’s shell length outermost ring to the shell margin. In order to at the beginning of the experiments is denoted as examine whether the ring on the shell surface was SLj (mm), then the shell length increment DSLj suitable for age determination, the marginal (mm) of the jth individual as derived by Gulland16 growth in each subsample was observed from can be written as

November 1999 to November 2000. - kDt DSLj = (SL• - SLj)(1 - e ) (1) where Dt is the elapsed time from the beginning to Field growth experiments the end of the experiment, which was 1 year. The least squares method was employed for estimating

To survey the seasonal growth of C. japonica, field k and SL• of equation (1). growth experiments were conducted from 6 To examine whether carving the shell surface November 1999 to 13 November 2000. Experimen- with a router had any effect on the survival and tal individuals were collected from Torigasaki the growth of MG individuals, the individuals that (Fig. 1) at Lake Shinji on 4 November 1999, where ranged from 10.1 mm to 24.9 mm in shell length fishing of C. japonica was prohibited. The shell were chosen as a control group and were not length (mm) and body weight (g) were measured numbered with the router. They were classified and these individuals were categorized into four into three groups with a shell length class at 5- groups (Table 1) as follows. mm intervals. Three groups, of which the shell

In order to observe the growth of individual length ranges were equal to those of MG1, MG2 specimens, 103 clams ranging from 10.8 mm to and MG3, were denoted as group 1 (G1), group 2 26.9 mm in shell length were sorted as the marked (G2) and group 3 (G3) in ascending order, respec- group (MG), which included four shell length tively. The number of individuals in each group classes. The sequential numbers were carved on was 200 (Table 1). In order to compare the survival rates and the shell length increments in these groups with those of the MG, the same observa- Table 1 Shell length range and number of individuals tions as for the MG were carried out on these in the marked and control groups three groups that were placed in the experimental Group Shell length SL (mm) No. individuals cage. Marked group In addition, the water temperature in the experiment site was observed two or four times a month MG1 10 £ SL < 15 30 MG2 15 £ SL < 20 30 from February to November 2000. The average MG3 20 £ SL < 25 30 water temperature calculated each month was MG4 25 £ SL 13 used as the water temperature for that month. The Control group water temperature before January 2000 was also G1 10 £ SL < 15 200 used, and it had been obtained from the monthly G2 15 £ SL < 20 200 monitoring surveys at Lakes Shinji and Nakaumi G3 20 £ SL < 25 200 by the Shimane Prefectural Freshwater Fisheries Experimental Station. 604 FISHERIES SCIENCE K Oshima et al.

RESULTS The peaks did not change from November 1999 to May 2000, but shifted to a larger shell length class Shell length distribution after May. Let us denote the three peaks of 0–1-, 7–8- and 17–18-mm shell length classes in May Monthly shell length distributions at Matsue and as small, medium and large classes, respectively. Kimachi are represented in Figs 2 and 3, respec- First, the large class did not shift to another class tively. Individuals over 5 mm in shell length were from May to July and disappeared after August. scarce from February to April 2000 and the fre- Second, the medium class suddenly shifted to a quency of shell length classes >20 mm was low larger class from May to July. However, this class throughout the year in both areas, compared to gradually moved to the upper class after August, individuals <20 mm. Furthermore, owing to our growing to the 16–17-mm shell length class in method for separating small clams from sedi- November. Finally, the small class shifted at a ments, the frequency of the <2-mm shell length slower rate than the medium class, although the class was considerably increased in February. The small class shifted to the larger class from May to number of individuals in the <5-mm shell length July, becoming the 6–7-mm shell length class in class remarkably diminished at both sampling October, which was found to continuously shift to sites, during July and August. a larger class from August to October. However, the At Matsue (Fig. 2), three obvious peaks of shell small class did not appear in November. In con- length appeared throughout the sampling period. trast, a new peak appeared in the 0–1-mm shell length class in September, and this new class frequency steeply increased until November. 2 2 '99. Nov. Aug. 1 1 n = 7,088 n = 5,930 2 2 0 0 '99. Nov. Jul. Dec. 1 1 1 4 n = 2,120 n = 3 ,448 n = 5,752 0 0 0 Sep. Dec. Aug. '00. Jan. 1 1 1 2 n = 11,545 n = 2,848 n = 5,896 n = 4,030 0 0 0 1 '00. Jan. 4 n ) 2 Feb. 0 = 4,320 2 0 n = 5,450 ) Sep. 2 /m 1 6 n 3 2 2 = 11,196 /m Feb.

0 3 1 n = 4,870 2 Mar. 4 Oct. n 0 0 1 n = 4,580 = 19,150 2 0 2 Mar. 1 n = 4,987 4 2 Apr. Oct. 0 1 n = 7,804 0 n = 14,544 2 2 0 8 Apr. n = 4 ,116 Number of individuals (10 1 2 May Number of individuals (10 0 0 1 n = 12,836 6 2 0 Nov. May n n = 27,810 1 = 5,216 4 2 Jun. 4 Nov. 0 1 n = 16,548 n = 10,508 2 2 0 2 Jun. n Jul. 1 = 7,104 1 n = 8,440 0 0 0 0 051015 20 25 05101520 25 051015 20 25 05101520 25 Shell length (mm) Shell length (mm)

Fig. 2 Monthly shell length distributions at Matsue in Fig. 3 Monthly shell length distributions at Kimachi in Lake Shinji. Lake Shinji. Growth and age of Corbicula japonica FISHERIES SCIENCE 605

The shell length distribution at Kimachi (Fig. 3) 80 was different from that at Matsue. There were no obvious peaks larger than 5 mm shell length from 40 '99. Nov. November 1999 to July 2000. However, as well as 0 the shell length distributions at Matsue, a notice- able peak appeared in the 0–1-mm shell length class 40 Dec. during the sampling period. The peak shifted to a larger class after May and moved to the 10–11-mm 0 shell length class in October, but was not found in 40 November. In addition, the new peak appeared in '00. Jan. the 0–1-mm shell length class in September. 0 40 Age determination Feb. 0 Figure 4 shows the marginal growth distributions 40 of subsamples with respect to the one-ring and Mar. two-ring groups and for ring groups with more 0 than three rings (3+-ring group), from November 1999 to November 2000. The marginal growth of 40 Apr. each ring group did not vary from November 1999 0 to May 2000, although in June the peaks of marginal growth of each ring group became the small- 40 May est marginal growth class in the sampling period, which ranged 1–2 mm, 0–1 mm and 0–1 mm in the 0 1-ring, 2-ring and 3+-ring group, respectively. The 40 marginal growth of the 1-ring group continuously Frequency (%) Jun. increased from July to November. In contrast, the 0 marginal growth of the 2-ring and 3+-ring groups did not vary from August to November, although 40 Jul. they increased from July to August. These facts 0 indicate that the new and outermost ring on the shell surface was formed once in the period from 40 Aug. November 1999 to May 2000 and was observed in 0 June. Thus, the ring on the shell surface was an annual ring and was available as a character for age 40 Sep. determination. Figure 5 represents the shell length distribution 0 of the outermost ring of the 1-ring, 2-ring and 3- 40 ring groups in the subsamples collected from July Oct. to November 2000 after the new ring was observed. 0 The shell lengths of the outermost ring in the 1-ring, 2-ring and 3-ring groups ranged 4–17 mm, 40 Nov. 9–20 mm and 13–23 mm, respectively, and formed 0 unimodal distributions. The mean shell length at each ring in the 024681012 subsamples is summarized in Table 2. Li (i = 1–7) Marginal growth (mm) indicates the shell length at the ith ring. Lee’s phenomenon was observed on the relationship of Fig. 4 Marginal growth distribution of the subsamples mean shell length to ring number. L2, L3, L4, L5 and collected from November 1999 to November 2000 at L6 in all ring groups with the exception of the 7-ring Matsue in Lake Shinji. Marginal growth frequency of the group diminished with the ring number. (····) 1-ring, (- - -) 2-ring and (––) 3+-ring groups.

Field growth experiments between the router-marked group and the non- marked group. The survival rates of MG, G1, G2 Before obtaining the results of the ﬁeld growth and G3 gradually decreased throughout the exper- experiments, we compared the survival rates imental period. The annual survival rates of MG1, 606 FISHERIES SCIENCE K Oshima et al.

MG2, MG3, MG4, G1, G2 and G3 were 73.3%, 83.3%, vary from November 1999 to April 2000, when the 80.0%, 84.6%, 76.5%, 86.5% and 70.0%, respec- water temperature was below 11∞C, but increased tively. There were no statistically significant differ- markedly from May to July when the water tem- ences of annual survival rates between MG1 and perature rose from 15∞C to 30∞C. The standard G1, MG2 and G2, and MG3 and G3, respectively, at deviation of the shell length increment also the 5% significance level. That is, the survival rate increased during this period. The mean shell of the MG was not affected by carving the shell length increments reached the maximum, which surface with a router. were 1.5 mm in MG1, 0.9 mm in MG2, 0.6 mm in Figure 6 represents the relationship of the mean MG3, and 0.3 mm in MG4, respectively, in July shell length increment per month (mm) in the MG when the water temperature was 26.9∞C. However, to the water temperature at Torigasaki in Lake the increment diminished during August when the Shinji. The mean shell length increment did not highest water temperature was recorded, which was 30.1∞C. As the water temperature dropped from September to November, the shell length 20 increment continued to decline. There was a significant correlation between the body weight 1-ring group increment and the shell length increment, where 10

0 2.5 Jul MG1 MG2 2.0 20 1.5 Jul 2-ring group 10 1.0 0.5 Feb Feb 0 0.0 Frequency (%) 2.0 MG3 MG4

20 per month (mm) 1.5 '00.Nov '00.Nov '99.Dec Jul '99.Dec 3-ring group 1.0

Mean shell length increment Jul 10 0.5 Feb Feb 0.0 0 0102030 0102030 051015 20 25 Water temperature (ºC)

Shell length (mm) Fig. 6 Relationship between the mean shell length increment per month (mm) in the marked group (MG;

Fig. 5 Shell length distributions of the outermost ring MG1, MG2, MG3 and MG4) to the water temperature in the 1-ring, 2-ring and 3-ring groups collected from recorded each month at Torigasaki in Lake Shinji. Vertical July to November 2000. error bars indicate standard deviation.

Table 2 Mean shell length (mm) at each ring of Corbicula japonica in Lake Shinji

Mean shell length Li (mm)

Ring group L1 L2 L3 L4 L5 L6 L7 No. individuals 1 10.0 358 2 8.3 15.4 375 3 7.7 14.6 17.8 341 4 7.5 13.0 16.4 18.8 102 5 8.1 13.1 16.1 18.6 20.4 37 6 8.6 13.0 15.8 18.0 19.7 21.3 12 7 9.4 14.7 17.5 19.0 20.9 21.9 22.8 1 Mean 8.6 14.7 17.3 18.7 20.3 21.3 22.8 Total 1226

Li (i = 1–7), shell length at the ith ring. Growth and age of Corbicula japonica FISHERIES SCIENCE 607

the correlation coefficient was 0.94 at the 0.1% sig- DISCUSSION nificance level. Thus, the seasonal variation in the mean body weight increment was very similar to Growth characteristics that in the shell length increment. The annual increments of mean shell length and mean body The seasonal change in the shell length distribu- weight were 4.8 mm and 1.2 g in MG1, 2.9 mm and tion at Matsue (Fig. 2) and the results of the field 1.1 g in MG2, 1.6 mm and 0.7 g in MG3, and 1.0 mm growth experiments (Fig. 6) explained the shell and 0.5 g in MG4, respectively. The growth rate in growth periodicity of C. japonica in Lake Shinji as the group with a shell length larger than 20 mm follows. That is, C. japonica did not grow in winter, decreased with increasing shell length. In contrast, grew rapidly from spring to early summer and then the annual increments of the mean shell length slowly from summer to autumn. In fact, the mean and the mean body weight were 4.5 mm and 1.3 g shell length increments of the MG were -0.1 mm, in G1, 2.5 mm and 1.0 g in G2, and 1.4 mm and 1.6 mm and 0.5 mm during those periods, respec- 0.7 g in G3, respectively. Accordingly, the annual tively. Similarly, the shell growth patterns for 11,13 increments of MG1, MG2 and MG3 did not differ C. japonica have been studied in other regions from those of G1, G2 and G3 in ascending order, and in other bivalves.4,17,18 Shell growth disturbance respectively. can be caused by high or low temperatures, sudden Figure 7 indicates the relationship of the annual weather changes, spawning, gonad development, shell length increment DSLj (mm) to the shell limited food supply or fishing activity such as clam 19–21 length SLj (mm) of the jth individual at the begin- dredging. Tanaka found that the growth rates of ning of the experiments. DSLj decreased linearly C. japonica juveniles reared in the laboratory did with SLj at the 1% significance level, P < 0.01 (coef- not change below 10∞C water temperature, but ficient of determination, 0.645). The growth coeffi- increased above 15∞C and, in particular, were the 22 cient k and the asymptotic shell length SL• were highest at 25–30∞C. The shell growth in the MG estimated from the shell length of the MG recorded group had a similar trend to those of juveniles from individually according to equation (1). Table 3 November 1999 to July 2000, but became slower shows the estimates of k and SL• of MG, which from August to November 2000 in spite of a water were 0.331/year and 28.2 mm, respectively. The temperature higher than 15∞C. In contrast, the 95% upper or lower confidence limits for them shell length class of the smallest peak in May were estimated to be 0.401/year or 0.263/year for k (Figs 2,3) obviously shifted to larger shell length and 30.0 mm or 26.9 mm for SL• with the bootstrap classes from June to October. The reproductive method. season of C. japonica in Lake Shinji was estimated to be from the middle of June to the middle of October, mainly from late June to late July (Naka- mura M & Harada S, pers. comm., 2001). In addi- 8 tion, all individuals with >15 mm shell length had already matured in Lakes Ogawara12 and Abashiri.23

(mm) Thus, most experimental individuals >15 mm shell j 6 length in June 2000 appeared to have already matured prior to the breeding season. In contrast,

4 Table 3 Estimates of the growth coefﬁcient k (per year)

and the asymptotic shell length SL• (mm) of Corbicula japonica 2 k SL• (per year) (mm) Latitude

0 Lake Shinji 0.331 28.2 35∞26 N Kando River10 0.115 50.9 35∞21 N 10 15 20 25 30 Lake Ogawara12 Shell length increment D SL SLj Southwestern area 0.250 36.1 40∞48 N Shell length (mm) Northwestern area 0.195 28.0 Lake Abashiri11 Fig. 7 Relationship between the annual shell length 1970–1972 year-classes 0.354 25.5 43∞57 N increment DSLj (mm) of jth individual to the shell length 1973–1975 year classes 0.106 58.0 SLj (mm) at the beginning of the ﬁeld growth experi- 1976–1978 year-classes 0.221 47.2 ments. (––) Regression line; (- - -) 95% conﬁdence limit. 608 FISHERIES SCIENCE K Oshima et al.

all individuals of the smallest peaks were immature number on the shell surface, because the first true at Matsue and Kimachi. Isono et al. inferred that ring on the shell surface formed a few months after Ruditapes philippinarum grew slowly at a water settlement and was rarely observable and could temperature higher than 25∞C due to decreased not be included in the ring counts.4 The obvious metabolic efficiency.24 The filtration rate of peaks in the 0–1-mm shell length class in Figs 2 and C. japonica declined at a water temperature higher 3 indicate the 2000 year-class, which was observed than 30∞C.14 In Lake Shinji, the water temperature from September to November 2000, because reaches temperatures higher than 30∞C in the sum- spawning begins from the middle of June. Because mer. Takada et al. referred to the gradual shell the peaks that appeared in the 0–1-mm shell length growth after summer of C. japonica in Lake Shinji; class from November 1999 to May 2000 can be the marginal shell growth did not increase rapidly regarded as the 1999 year-class, the medium peak during autumn, whereas the soft tissue weight in in May (Fig. 2) was considered to be the 1998 year- each ring group increased during the same period.9 class. The shell length distribution of the outer- They inferred from this fact that the majority of most ring in the 1-ring group of the subsamples energy taken in was mainly allocated to recovering collected after the new growth ring was observed the soft tissue weight that had been decreased due (Fig. 5) was almost similar to the shell length dis- to the discharge of reproductive material during tribution in the 5–15-mm classes in May (Fig. 2). the breeding season. In the present study, the sea- Consequently, the first growth ring apparently sonal changes of soft tissue weight were not exam- observed on the shell surface of C. japonica in Lake ined, but the mean shell length increment of the Shinji is formed during the second year after set- MG dropped after the main breeding period. This tlement. That is, if the spawning and settlement fact suggests that the shell growth decrease during have been completed by November, the age of summer is caused by the stress of high water clams in the i-ring group at the time when the shell temperature and as a result of being in the post- growth resumes in May is i + 0.5 (i = 1, 2, · · ·). The spawning stage, and the gradual shell growth in shell length of juveniles of C. japonica at the first autumn is due to the recovery of soft tissue weight shell growth rest (which were reared at the same after the breeding period. Thus, the shell growth of water temperature variations as in Lake Shinji), C. japonica in Lake Shinji is not only affected by ranged from 0.28 mm to 2.37 mm in shell length the water temperature but also by physiological and was on average 0.90 mm (Nakamura M & activity. Harada S, pers. comm., 2001). Additionally, the peak of the 1999 year-class was observed in the 1– 2-mm shell length class in June, when shell growth Age determination was resumed (Figs 2,3). The first true growth ring on the shell surface is formed at 1–2 mm shell The growth ring on the shell surface of C. japonica length, although it is resolved with growth. Accord- in Kando River and Lake Abashiri is formed during ingly, the age determined by Kawashima et al. and winter.10,11 As described here, C. japonica in Lake Utoh is probably underestimated, because they did Shinji grew from spring to autumn. In addition, the not confirm that the apparent first growth ring on marginal growth of all ring groups (Fig. 4) was min- the shell surface was the first true growth ring.10,11 imal at the beginning of June before reproduction Lee’s phenomenon was observed in the age occurred. Thus, the growth ring of C. japonica in determination results from subsamples (Table 2). Lake Shinji indicates shell growth cessation due to This phenomenon was found in Haliotis discus dis- low water temperature in winter, which then cus at Tokushima, Japan.25 Fishery-induced size- resumes rapidly in spring. We conclude that the selective mortality, which removes larger and faster growth ring was formed once a year in winter for growing individuals from a population, reduces the

C. japonica in Lake Shinji. parameters k and SL• in the von Bertalanffy growth Kawashima et al. and Utoh regarded the first equation.26,27 Fahy et al. considered that a low esti- growth ring on the shell surface as being the ring mate of SL• for Spisula solida at Clifden, Ireland, formed during the first year after settlement.10,11 In which was heavily fished, was attributed to Lee’s contrast, the second growth line observed in the phenomenon.8 Because the C. japonica population acetate peel replica of the shell section was often is heavily exploited in Lake Shinji, both parameters perceived as the first growth line of C. japonica in were not estimated from the subsamples collected Lake Ogawara, because the shell surface at the in the fishing grounds but from the annual shell adjacent umbonal region that included the first length increments in the MG, of which individuals true growth line was eroded in most of the large- were collected in the prohibited fishing area. and medium-sized clams.12 Ansell determined the Table 4 shows the shell length of each ring group age of Venus striatula by adding one half to the ring determined from the concentric groove and the Growth and age of Corbicula japonica FISHERIES SCIENCE 609

Table 4 Mean shell length (mm) at each ring of Corbicular japonica in Lake Shinji

Mean shell length Li (mm)

Site L1 L2 L3 L4 L5 L6 L7 References Matsue† 8.6 14.7 17.3 18.7 20.3 21.3 22.8 Present study Tamayu‡ 10.3 15.5 18.0 19.9 21.3 22.0 Takada et al.9 Hikawa‡ 12.4 17.0 20.2 Takada et al.9

Li (i = 1–7), shell length at the ith ring. †Shell length is measured from the concentric groove. ‡Shell length is measured from the chromatic growth ring. chromatic growth ring used for the age determina- France.29 However, there was no significant corre- tion character by Takada et al. on the shell surface.9 lation between the estimates of k and latitudes in They noted that the chromatic growth ring was rec- Table 3 at the 5% significant level. Consequently, ognized after shell growth resumed in spring. the growth rate of C. japonica is affected by other There was also a difference of shell length at each conditions such as the availability and quantity of ring between Tamayu and Hikawa. There were no food or habitat density as well as latitude. differences in L2, L3, L4, L5 and L6 between Matsue In order to establish fishery resource manage- and Tamayu, with the exception of L1. The chro- ment, it is essential to clarify the population matic growth ring on the shell surface was, how- dynamics of target species. The present study has ever, not necessarily observed in all individuals assessed the growth characteristics of C. japonica and they were often unclear or could not be recog- in Lake Shinji and has demonstrated the availabil- nized. Because the concentric groove was found in ity of the concentric groove on the shell surface for most clams, it is suitable for age determination. age determination and the relationship of the ring number to age. These results will yield important information on the population dynamics of this

Comparing k and SL•• commercially important species.

Table 3 represents the estimates of the growth coefficient and the asymptotic shell length of ACKNOWLEDGMENT C. japonica in Lake Shinji, Kando River,10 Lake 12 11 Ogawara and Lake Abashiri, , respectively, with We wish to express our sincere thanks to the the respective latitudes of the four regions. The two members of the Shimane Prefectural Freshwater sets of k and SL• in Lake Ogawara were estimated Fisheries Experimental Station for their help. in consideration of the growth difference between south-western and north-western areas of this lake. At Lake Abashiri, Utoh estimated k and SL• for the 1970–1972, 1973–1975 and 1976–1978 year- REFERENCES classes, because there were differences in growth among year-classes due to the annual fluctuation 1. Nakamura M, Ohkita S, Harada S. Report of research on 11 population size assessment of Corbicula japonica in Lake of growth rate. While the estimate of k in Lake Shinji. Bull. Shimane Pref. Freshwater Fish. Exp. Stn 2003; 4: Shinji was the largest in the regions with the excep- 112–116 (in Japanese). tion of Lake Abashiri (1970–1972 year-classes), the 2. Orton JH. On the rate of growth of Cardium edule. Part I. estimate of SL• in Lake Shinji was smaller than Experimental observations. J. Mar. Biol. Assoc. U.K. 1926; those of other regions except for Lakes Ogawara 14: 239–279. (northwestern area of lake) and Abashiri (1970– 3. Stevenson JA, Dickie LM. Annual growth rings and rate of 1972 year-classes). This fact indicates that growth of the giant scallop, Placopecten magellanicus C. japonica in Lake Shinji grew more rapidly and (Gmelin) in the Digby area of the Bay of Fundy. J. Fish. Res. attains the asymptotic shell length at an earlier age Board Can. 1954; 11: 660–671. than in other regions. Taylor found negative and 4. Ansell AD. Reproduction, growth and mortality of Venus striatula (Da Costa) in Kames Bay, Millport. J. Mar. Biol. positive correlations between temperature and lat- Assoc. U.K. 1961; 41: 191–215. itude, and temperature and the growth coefficient, 5. Goshima S, Noda T. Shell growth of the North Pacific cockle respectively, for Siliqua patula in the north-east Clinocardium californiense in Hakodate Bay, Hokkaido. 28 Pacific. In addition, Bachelet showed that the Benthos Res. 1992; 42: 39–48. growth coefficient was negatively correlated with 6. Nakaoka M. Age determination and growth analysis based latitude for Macoma balthica in south-west on external shell rings of the protobranch bivalve Yoldia 610 FISHERIES SCIENCE K Oshima et al.

notabilis Yokohama in Otsuchi Bay, northeastern Japan. Bay, Japan, with reference to the influence of food supply Benthos Res. 1992; 43: 53–66. from the water column. Mar. Ecol. Prog. Ser. 1992; 88: 215– 7. Sakurai I. Age and growth of the sunray surf clam Mactra 223. chinensis in Tomakomai, Southwest Hokkaido. Nippon 19. Ramon M, Richardson CA. Age determination and shell Suisan Gakkaishi 1993; 59: 469–472. growth of Chamelea gallina (Bivalvia: Veneridae) in the 8. Fahy E, Carroll J, O’Toole M, Hickey J. A preliminary account western Mediterranean. Mar. Ecol. Prog. Ser. 1992; 89: 15– of fisheries for the surf clam Spisula solida (L) (Mactracea) 23. in Ireland. Fish. Bull. (Dublin) 2003; 21: 1–27. 20. Gasper MB, Richardson CA, Monteiro CC. The effects of 9. Takada Y, Sonoda T, Nakamura M, Nakao S. Growth and dredging on shell formation in the razor clam Ensis siliqua settlement of the Bivalve, Corbicula japonica population in from Barrinha, southern Portugal. J. Mar. Biol. Assoc. U.K. Lake Shinji. Nippon Suisan Gakkaishi 2001; 67: 678–686. 1994; 74: 927–938. 10. Kawashima T, Yamane Y, Yamamoto K. Growth of the 21. Gasper MB, Castro M, Monteiro CC. Age and growth rate of brackish water bivalve Corbicula japonica in Kando River the clam, Spisula solida L., from a site off Vilamoura, south and difference in proportion between C. japonica in Kando Portugal, determined from acetate replicas of shell sections. River and Lake Shinji. Rep. Shimane Pref. Fish. Exp. Stn Sci. Mar. 1995; 59 (Suppl. 1): 87–93. 1988; 5: 94–102 (in Japanese). 22. Tanaka Y. Morphological and physiological characteristics 11. Utoh H. Growth of the brackish-water bivalve, Corbicula of the post larval stages in Corbicula japonica Prime, reared japonica Prime, in Lake Abashiri. Sci. Rep. Hokkaido Fish. in the laboratory. Bull. Natl Res. Inst. Aquacult. 1984; 6: 23– Exp. Stn 1981; 23: 65–81. 27. 12. Fuji A. Ecology and stock of the brackish water bivalve Cor- 23. Maru K. Reproductive cycle of the brackish-water bivalve, bicula japonica in Lake Ogawara. Comprehensive report. Corbicula japonica, in Lake Abashiri. Sci. Rep. Hokkaido In: Report of Research on Fisheries in Lake Ogawara. Final Fish. Exp. Stn 1981; 23: 83–95. Comprehensive Study. Construction Office for the Compre- 24. Isono RS, Kita J, Kishida C. Upper temperature effect on hensive Development of the Takase River of Tohoku rates of growth and oxygen consumption of the Japanese Regional Construction Bureau, Aomori. 1997; 33–73 (in littleneck clam, Ruditapes philippinarum. Nippon Suisan Japanese). Gakkaishi 1998; 64: 373–376. 13. Fuji A. Growth and breeding season of the brackish-water 25. Kojima H, Nakahisa Y, Tanimoto H, Isibasi K. A study on the bivalve, Corbicula japonica, in Zyusan-gata Inlet. Bull. Fac. stock of Japanese black abalone, Haliotis discus discus in Fish. Hokkaido Univ. 1957; 8: 178–184. Tokushima Prefecture – I. Growth of Shells. Bull. Tokai Reg. 14. Nakamura M. Physio-ecological study on interrelationships Fish. Res. Lab. 1977; 90: 25–37. between Corbicula japonica Prime and environment in 26. Ricker WE. Effects of size-selective mortality and sampling Lake Shinji, Japan. Rep. Shimane Pref. Fish. Exp. Stn 1998; 9: bias on estimates of growth, mortality, production and 1–192 (in Japanese). yield. J. Fish. Res. Board Can. 1969; 26: 479–541. 15. Sellmer GP. A method for the separation of small bivalve 27. Vaughan DS, Burton ML. Estimation of von Bertalanffy molluscs from sediments. Ecology 1956; 37: 206. growth parameters in the presence of size-selective mortal- 16. Gulland JA. Fish Stock Assessment: A Manual of Basic ity: a simulated example with Red Grouper. Trans. Am. Fish. Methods. John Wiley and Sons, New York. 1983. Soc. 1994; 123: 1–8. 17. Jones DS, Williams DF, Arthur MA. Growth history and ecol- 28. Taylor CC. Temperature and growth – the Pacific razor clam. ogy of the Atlantic surf clam, Spisula solidissima (Dillwyn), J. Cons. Int. Explor. Mer. 1959; 25: 93–101. as revealed by stable isotopes and annual shell increments. 29. Bachelet G. Growth and recruitment of the tellinid bivalve J. Exp. Mar. Biol. Ecol. 1983; 73: 225–242. Macoma balthica at the southern limit of its geographical 18. Nakaoka M. Spatial and seasonal variation in growth rate distribution, the Gironde estuary (SW France). Mar. Biol. and secondary production of Yoldia notabilis in Otsuchi 1980; 59: 105–117.