Fisheries Science (2019) 85:465–474 https://doi.org/10.1007/s12562-019-01297-0

ORIGINAL ARTICLE

Biology

Reproductive cycle and growth of the Scaphechinus griseus inhabiting Japanese surf clam Pseudocardium sachalinense fshing grounds in Tomakomai, southwest Hokkaido, Japan

Izumi Sakurai1 · Honami Abe1 · Takashi Ogata2

Received: 1 September 2018 / Accepted: 30 January 2019 / Published online: 13 February 2019 © Japanese Society of Fisheries Science 2019

Abstract Bioturbation by the sand dollar Scaphechinus griseus is suspected to inhibit the recruitment of Pseudocardium sachalinense, a commercially important bivalve. This study aimed to develop a standard method for the extermination of the sand dollar by examining its reproductive cycle, relationships between age and growth, and population structure in Tomakomai, southwest Hokkaido, Japan. Histological observations of the gonads indicated that the sand dollar has one spawning season per year, in June–August. Seasonal changes in the appearance of a dark band around the interambulacral plate suggested that the annual ring primarily forms in June–July, with the frst ring forming at 1 year of age. Analysis of ftness by growth models showed that the Gompertz curve was better matched to the data than the von Bertalanfy and logistic curves; growth is fast until 1.6 years of age, then slows. The population density was 190–257 individuals/m2, and average test diameters were 39.0–40.9 mm. Three-year-olds comprised the highest percentage of the population; no individuals of 8 years of age or older were detected. In conclusion, to reduce the density of sand dollars efciently and to prevent their reproduction, individuals with a test diameter of over 30 mm should be exterminated before the spawning season.

Keywords Age determination · Population structure · Recruitment · Fitness · Gompertz curve · Extermination

Introduction (Takamaru 1984; Hayashi 1988; Sakurai et al. 1991), predation by moon shells and sea stars (Hayashi et al. 1962; Takamaru The Japanese surf clam Pseudocardium sachalinense fshery 1984), and, possibly, exclusion due to interspecifc competition had an annual catch of 651–741 tons from 2010 to 2016 in (Hayashi et al. 1962). There remains controversy over whether Tomakomai, southwest Hokkaido, Japan. Production of this bioturbation caused by the burrowing and feeding actions of clam during this period was the highest recorded in Japan the sand dollar Scaphechinus griseus, the habitat of which since 2000. However, the abundance of this clam has exhib- overlaps with that of P. sachalinense, infuences the survival ited a continuous decline in Tomakomai since 2008, due to of juvenile clams (Hayashi et al. 1963; Sakurai et al. 2003). a decline in recruitment. The sand dollar S. griseus is an irregular deposit-feeding Factors contributing to this decline include fuctuation in echinoid that belongs to the family Scutellidae. This species recruitment, changes to fertility and subsequent larval supply is widely distributed on the upper subtidal sandy bottom of (Hayashi et al. 1967; Sakurai and Nakao 1996), the dislodge- the coast of northern Japan, including the regions of Hok- ment of juvenile clams due to wave action and tidal currents kaido, Sakhalin, and Kurile Islands (Utinomi 1960; Drozdov and Vinnikova 2010). Sand dollars form dense beds over a period of several decades (Chia 1969; Merrill and Hobson * Izumi Sakurai [email protected] 1970; Birkeland and Chia 1971; Parks 1973; Niesen 1977), and these beds have been detected along several parts of the 1 School of Biological Science, Tokai University, Sapporo, coast of Hokkaido (Hayashi et al. 1962; Takamaru 1983; Hokkaido 005‑8601, Japan Sakurai et al. 1991, 2001, 2003). Several studies have shown 2 Hokkaido Aquaculture Promotion Corporation, Sapporo, that bioturbation by sand dollars infuences the structure of Hokkaido 003‑0874, Japan

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meiobenthic and microphytobenthic communities (Findley ° ° 140 E 145 E N and White 1983; Creed and Coull 1984; Reidenauer 1989; 45°N Okhotsk Sea Li et al. 2013; Brustolin et al. 2016). In particular, adult S. The Sea of mirabilis individuals are able to kill newly settled juveniles Japan by their bioturbation activity (Takeda 2008). Furthermore, a Pacific Ocean 42°N prawn fshery operation using bottom trawling was adversely Tomakomai Tomakomai afected by large numbers of S. mirabilis entrapped in the net due to a huge outbreak of the sand dollar in Fukuoka and Tomakomai River → Motomachi ← Koitoi River Ehime prefectures (Matsuda et al. 2008). Ariake Whether bioturbation by S. griseus is causing fuctuations in the number of newly settled P. sachalinense remains sub- Tomakomai West Port 5m ject to debate; however, clam fshermen in Hokkaido have 0 1km carried out maintenance of the fshing grounds by extermi- 10m nating the sand dollar. However, a standard method to ensure the efective extermination of the sand dollar is required, in Fig. 1 Location of the survey area of the coast of Tomakomai, south- particular with regard to how many should be exterminated west Hokkaido, Japan. Shaded rectangle indicates the sampling area and in what season. At present, only haphazard extermina- for gonad observation and growth analysis of Scaphechinus griseus. Open square represents the sampling area that contained stations tion is carried out, in which sand dollars are landed at the (Stns) 1–5 for analyzing the density and age structure of the popula- same time as clams during fshing. Therefore, it is necessary tion. Open circle indicates the position of an embedded water tem- to examine the mechanisms of the formation and mainte- perature data logger nance of the S. griseus population, as well as establishing the population density that afects newly settled juvenile clams. Observation of the gonadal developmental process At present, the life history traits of the sand dollar, includ- ing growth and reproduction, are not known, and even the After the samples were rinsed with tap water and the water density of the population in Tomakomai has not been clari- was wiped off, the test diameter (i.e., the length of the fed. Therefore, this study examined the annual reproduc- antero-posterior axis across the peristome) was measured tive cycle, relationship between age and growth, population ± 0.01 mm using a digital vernier caliper (N20; Mitsutoyo, density, and age structure of S. griseus in Tomakomai, Japan. Kawasaki, Japan). The total weight (TW) of the specimens was measured to ±0.01 g by an electronic balance (GH252; A & D, Tokyo). Five gonads were then extracted using Materials and methods tweezers after removing the skeletal plates of the aboral side. It was extremely difcult to remove only the gonads Study site and sampling method completely because the gonads develop to cover the gut and bury the gap of the peripheral calcite buttress system and the diverticular pouches. Therefore, the gonads and gut Sand dollar S. griseus individuals that had a test diameter were removed together (GW) and were weighed together to greater than 30 mm were collected at 5- to 7-m depth of ±0.01 g on the electronic balance after washing the gut con- Ariake in Tomakomai, Hokkaido (42°37′N, 141°36′E; tents with tap water. The gonad index (= GW / TW × 100) Fig. 1), which is the same area where S. griseus individuals was then calculated. A small piece of approximately 5 mm are primarily distributed (Sakurai et al. 1991). Samples were cube was cut of the central part of the weighed gonad and collected from December 2016 to November 2017 using a dehydrated. After normal parafn embedding, serial sections hydraulic jet dredge (width, 1.2 m; mesh size of net bag, were prepared at 6-µm thickness and stained with Mayer’s 90 mm; spacing of teeth, 36 mm; angle of tooth, 60°) that was hematoxylin and eosin. Then, histological observation of the towed parallel to shore for a distance of 50–100 m. Thirty development process of the gonads was carried out under individuals were randomly selected every month as speci- a biological microscope (×400; CH30; Olympus, Tokyo). mens for gonadal observation and growth analysis, respec- tively. These individuals were preserved in 10% bufered for- Analysis of age and growth malin in the feld. In addition, 43 juvenile sand dollars were collected with a Smith-McIntyre grab sampler (i.e., not by Seasonal changes to the growth of the skeletal plate of echi- dredging; sampling area, 0.05 ­m2; sampling depth, approxi- noids often result in changes to the light and dark bands on mately 10 cm) at 5-m depth in the same area in May 2017 and the plate due to diferent growth rates between the warm September 2017. These individuals were used for the growth and cold seasons (Birkeland and Chia 1971; Pearse and analysis after preserving them in 5% bufered formalin.

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Pearse 1975; Brykov and Parasyna 1978; Kang et al. 2007). the outer edge of the interambulacral plate by using samples In particular, the dark band has been previously used for age with three rings. The age of the frst ring was estimated by determination because it is present in many echinoids as an the relationship between the test diameter and the number annual ring that is formed when the growth rate decreases. of the rings of S. griseus with a test diameter of < 20 mm By observing the plate of S. griseus under a biological that were collected in May 2017 and September 2017. We microscope before starting this study, it was confrmed that then determined the age (t) of the sand dollars based on a lighter zone is present in the center of the plate, with dark the spawning season, which was clarifed by observing the and light bands of similar shape forming alternately outside gonads. of the zone (Fig. 2). Therefore, we assumed that the dark The parameters ­TDmax, K, and c in the von Bertalanfy, bands formed a ring structure on the plate, and we performed Gompertz, and logistic growth curves, respectively, were an analysis to clarify the relationship between the age and evaluated with TD and t by maximum likelihood estima- growth of S. griseus. tion, using Microsoft Ofce Excel Solver Add-in according After the formalin-preserved samples for the growth anal- to Gorie (2001). ysis were rinsed with tap water and the water was wiped For the Von Bertalanfy curve, of, the test diameter (TD) was measured to a precision of −K(t−c) TD = TDmax(1 − e ). 0.01 mm using the caliper. Then, in accordance with Jensen (1969), the aboral surface of the sand dollar was polished For the Gompertz curve, using a whetstone and charred on a hot plate. The sides were −ce−Kt TD = TDmaxe . then cleaned in xylene to enhance the contrast between the light and dark bands on the plate before observing the ring For the logistic curve, structure under a stereo microscope (×40; SZ40; Olympus). TD TD = max . Although Jensen (1969) used the annual ring that formed 1 + e−K(t−c) on the genital plates, we used interambulacral plates, which K are lined up in the direction of the anus, because the genital where TD­ max is the theoretical maximum test diameter, is plate of S. griseus is very fragile. In addition, the interam- the growth coefcient, and c is the theoretical test diameter bulacral plate is easier to polish uniformly as it is closer to at age 0. The optimal model was statistically selected by the genital plate, and the ring structure near the outer edge Akaike information criterion (AIC). is easier to identify as it is closer to the anus. We determined Analysis of population density and age structure that the fourth interambulacral plate best satisfed the above two conditions; it was on the left towards the anus when counting from the genital plate (Fig. 2). Furthermore, we According to a report on the distribution of S. griseus in evaluated the formation period of the ring structures by cal- Tomakomai (Sakurai et al. 1991), the sand dollars is only culating the monthly ratio of the dark band formed around found at a depth of 5–7 m, and has a similar population

6th IP→ a to anus b

5th IP→

←5th ring ←4th ring 4th IP→ ←3rd ring ←2nd ring 3rd IP→ ←1st ring

2nd IP→

1st IP→ GP 1 mm 1 mm

Fig. 2 Photograph of the interambulacral plates (IP) with annual rings of the aboral test of S. griseus (a), and the fourth plate located on the left towards the anus from the genital plate (GP) (b) for which measurements were made

1 3 468 Fisheries Science (2019) 85:465–474 density throughout the year. In addition, the extermination Mellitidae, the gonadal developmental process was divided of S. griseus has not been carried out since 2006, when it into fve gametogenetic stages as follows. was undertaken of the coast of Motomachi in Tomako- Growth stage (Fig. 3a, b): the genital tubule is flled with mai. Therefore, sampling was carried out at 5-m depth of nutritive phagocytes. In females, the pre- and vitellogenic Motomachi in Tomakomai (Fig. 1) during May 2017. A oocytes have an irregular shape and appear to be attached diver arranged a rectangular frame (1 m in length × 1 m to the tube wall. In males, the spermatocytes occur near the in width) at fve random locations (stations 1–5) on the tube wall. seabed, and captured all sand dollars in the frame by hand. Premature stage (Fig. 3c, d): in females, a large number The obtained specimens were fxed with 10% bufered for- of mature oocytes are present, although vitellogenic oocytes malin. The rings on the interambulacral plate were counted are still present on the tube wall. In males, spermatocytes by the same procedure as described previously. form a narrow band near the tube wall, and spermatozoa fll the center of the genital tubule. Mature stage (Fig. 3e, f): in females, most of the genital Measurement of water temperature tubule is flled with mature oocytes and nutritive phagocytes are absent. In males, most of the genital tubule is flled with A data logger (StowAway Tidbit; Onset Computer, spermatozoa, although spermatocytes are still present near Bourne, MA) was buried at 5-m depth in Ariake (Fig. 1) the tube wall. and the water temperature recorded at 10-min intervals Spent stage (Fig. 3g, h): few oocytes and spermatozoa from December 2016 to November 2017. were found in the genital tube or in a reduced genital tubule. Resting stage (Fig. 3i, j): the genital tube is flled with nutritive phagocytes. The sex may be determined from the Results nutritive phagocytes, which have dense granules in females, and by spermatogonia adhering to the glass slide in males. Annual reproductive cycle Monthly changes in the composition of the gametogenetic stages are shown in Fig. 4. All female individuals were at Based on the gametogenic process of Mellita quinquiesper- the resting stage in December 2016, and 6% of individuals forata (Tavares and Borzone 2006), which belongs to family were at the growth stage in January 2017. In February 2017,

a c e g i ↖ GN NP ↘ MO ↙ ↖ VO MO ↘ ↗ GT

b d f h j ↗ GT ↖ SZ SZ SG ↘ ↙

↗ SC

Fig. 3 Gametogenetic stages in S. griseus. a, b growth stage; c, d pre- cyte, SC spermatocyte, SG spermatogonia, SZ spermatozoa, VO vitel- mature stage; e, f mature stage; g, h spent stage; i, j resting stage. GN logenic oocyte. Female (upper) and male (lower). Scale bars repre- Granules, GT genital tube, MO mature oocyte, NP nutritive phago- sent 200 µm and applies to all photographs

1 3 Fisheries Science (2019) 85:465–474 469 a total of 92% of individuals entered the growth stage and 20 7% of individuals entered the premature stage. Individuals began to enter the mature stage in April 2017, with 90% of ) 15 individuals at this stage in May 2017. From June to August 2017, a total of 88–100% of all individuals were at the spent 10 stage. However, in September 2017, individuals began to enter the resting stage, with 83% of individuals in the resting

Gonad index (% 5 stage by October 2017. In November 2017, all individuals shifted to the resting stage. 0 In comparison, the males of all individuals were at the Dec JanFeb MarApr MayJun JulAug Sep Oct Nov resting stage in December 2016. Between January and Feb- Month (2016-2017) ruary 2017, individuals at the growth stage increased from 29 to 82%. In March 2017, a total of 94% of individuals Fig. 5 Monthly changes in the gonad index of S. griseus from entered the premature stage. Individuals began entering the December 2016 to November 2017. Values are means. Shaded bars mature stage in March 2017, with all individuals being in the female gonad index, solid bars male gonad index, error bars SDs. Numbers of specimens are the same as shown in Fig. 4 mature stage in May. From June to August 2017, more than 92% of individuals were in the spent stage. From September to October 2017, a total of 39–78% of individuals entered Age and growth the resting stage. In November 2017, all male individuals were at the resting stage, similar to females. Monthly changes to the proportion of S. griseus with rings Monthly changes to the gonad index are shown in Fig. 5. forming around the outer edge of the interambulacral plate For both males and females, the gonad indices decreased are shown in Fig. 6. Although ring formation was observed from December 2016 to January 2017, then started to in individuals throughout the survey, these percentages increase in February 2017 and peaked in May 2017 (females, increased from April to June and July 2017, and then 16.1%; males, 15.7%), and decreased in June. This index decreased by November. In particular, 95–96% of individu- ranged from 6.3 to 8.0% and from 6.6 to 7.7% for females als had a ring around the interambulacral plate in June and and males, respectively, from June to September 2017. From July 2017. Thus, it was estimated that one annual ring is October 2017, the index for both sexes decreased to less than formed from June to July in the plates. Furthermore, the 5%. In addition, the sharp decrease in the gonad indices, as number of the rings could be converted to give the age of an observed in June 2017, was consistent with the spent stage individual because the period of ring formation coincided of the developmental process of the gonads. with the spent stage detected in the survey. Table 1 shows the test diameter and the number of rings of juvenile S. griseus with a test diameter of < 20 mm that were collected in May and September 2017. In May, two juveniles with test diameters of 9.7 and 15.1 mm, each with one and two rings, were collected. In September, six n =191613121310161613121220 100 80 60 n =182120221922242123212420 100 40

(% ) 20 Female 0 80 n =11 14 17 18 17 20 14 14 17 18 18 10 )

100 (% 60 80

Proportion 60 40

40 oporon

20 Male Pr 0 20 DecJan Feb Mar AprMay JunJul AugSep Oct Nov

Month (2016-2017) 0 DecJan FebMar AprMay JunJul AugSep OctNov Month (2016-2017) Fig. 4 Monthly changes in the relative proportion of S. griseus at each gametogenetic stage from December 2016 to November 2017. Open bars resting stage, shaded bars growth stage, checkered bars Fig. 6 Monthly change to the proportion of S. griseus with rings premature stage, solid bars mature stage, dotted bars spent stage. formed around the outer edge of the interambulacral plate. Numbers Numbers above bars indicate the number of specimens above points indicate the number of specimens

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Table 1 50 Test diameter and Month Test Number number of rings of juvenile diameter of rings Scaphechinus griseus collected (mm) 40 at 5- to 7-m depth of Ariake, Tomakomai, Japan during May May 2017 9.7 1 30 and September 2017 15.1 2 Sep 2017 3.3 − 20

5.4 − st diameter (mm) 10 6.6 − Te 9.7 1 0 9.9 1 01234567 10.7 1 Age (year)

Fig. 7 Relationship between the age and test diameter using von Bertalanfy (broken line), Gompertz (solid line), and logistic growth juveniles with test diameters of 3.3–10.7 mm were collected. curves (dotted line) of S. griseus in Tomakomai, Japan. A total of 374 Three of the individuals with test diameters of < 6.6 mm specimens were used for the age determination were too fragile for age analysis, while a single ring was found in other juveniles with test diameters of > 9.7 mm. Three juveniles with test diameters of < 6.6 mm in Septem- Population density and age structure ber were estimated to be less than 1 year old in June–August 2017 because they were smaller than the minimum juvenile Figure 8 shows the age compositions of S. griseus collected size in May. It is reasonable to suggest that the juvenile that from fve locations of Motomachi in Tomakomai, Japan. had a test diameter of 9.7 mm in May was almost 1 year old The population density and mean test diameter of the sand in June–August 2016, and that the three juveniles with test dollars are shown in Table 2. The values were highest for diameters of > 9.7 mm in September were 1 year old. Since a 3-year-old individuals at each station, and lowest for the single ring was confrmed in juveniles with test diameters of 7-year-old individuals. No sand dollars of ≥ 8 years of age 9.7 mm in May and > 9.7 mm in September, it is estimated were detected. The population density and the average test that the frst ring structure of S. griseus is formed at an age diameter were in the range of 190–257 individuals/m2 and of around 1 year old. 39.0–40.9 mm, respectively. The growth curves based on the above results for the ini- tial date of assessment on 1 June are as follows. Monthly changes to water temperature For the Von Bertalanfy curve, 0.506 t 0.652 TD = 44.2 1 − e− ( − ), Monthly changes to the water temperature of Motomachi in Tomakomai are shown in Fig. 9. The minimum and maxi- for the Gompertz curve, mum water temperatures were 4.0 °C in February 2017 and 0.769t TD = 42.3e−3.337e− . 18.8 °C in August. The water temperature rose from March to August 2017, exceeding 12 °C in June 2017 and 17 °C in For the logistic curve, July 2017, and then declined by November 2017. 41.5 TD = . 1 + e−1.002(t−2.040) Discussion The relationship between age and the test diameter of a total of 374 specimens used for the age determination This study demonstrated that, of the coast of Tomakomai, is shown in Fig. 7, together with each growth curve. The the gonadal development process of S. griseus had an annual test diameter and the age of S. griseus were in the range cycle that shifted to the growth stage in February, the pre- of 9.7–46.8 mm and 1–6 years old, respectively. The AIC mature stage in March, the mature stage in April–May, the value of the growth curve is lowest for the Gompertz curve spent stage in June–September, and the resting stage in (= 1718.1) and highest for the logistic curve (= 1724.3). The October–January. In parallel, the gonad index peaked in May AIC value of the von Bertalanfy curve is 1719.6. Because and decreased in June, indicating that the gonadal devel- the infection point of the Gompertz curve is TD = 15.6 mm opment process shifted from the mature stage in May to at t = 1.6 years, it is suggested that the growth rate of S. gri- the spent stage in June. These data indicate that the spawn- seus reached its maximum at 1.6 years of age and gradually ing season of S. griseus of the coast of Tomakomai peaks decreased thereafter. once a year in June–August. Furthermore, because the water

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50 related species (National Astronomical Observatory 2006) Stn. 1 showed that the spawning season of Astriclypeus manni, 25 n =220 which belongs to family Astriclypeidae, occurs in August in Chiba Prefecture, July–August in Kanagawa Prefecture, and

0 April–June in Ehime Prefecture. Furthermore, the spawning 50 season of japonicus, which belongs to family Stn. 2 , occurs in June–July in Ishikawa Prefecture, June–August in Chiba Prefecture, May–July in Kanagawa 25 n =218 Prefecture, May–September in Shizuoka Prefecture, June–September in Wakayama Prefecture, and May–June 0 in Kochi Prefecture. All of these spawning seasons generally 50 (% ) occur during the period when the water temperature rises, Stn. 3 regardless of species and region. Although it was not clear n =199 25 how water temperature is involved in the reproductive cycle of S. griseus in this study, the switch between the develop- Percentage 0 mental phase of gametes (i.e., from the growth to the spent 50 stages) and the nutrient storage phase (i.e., the resting stage) Stn. 4 of the sand dollar might be regulated by changes in the water n =190 25 temperature. In this study, we used the weight of the gonad together 0 with the gut to calculate the gonad index. Since the gut of S. 50 griseus is very thin and a seasonal change in its volume was Stn. 5 not observed with the naked eye during the measurement n =257 25 process, we consider that there was not any undue infuence of gut weight on the changes in the gonad index. Observations of the dark band that formed around 0 1 234567 the outer edge of the interambulacral plate revealed that S. griseus Age (year) the annual rings of are primarily formed in June–July, corresponding to the spent stage. The rela- tionship between the test diameter and the ring forma- Fig. 8 Age compositions of S. griseus collected from fve locations at 5-m depth of Motomachi, Tomakomai, Japan tion of the juveniles collected in May and September in Tomakomai suggested that the frst ring of S. griseus is formed in May of the year following spawning. There- temperature of the coast of Tomakomai increased from Feb- fore, we assumed that the frst annual ring of S. griseus ruary to August and decreased from August to February, it occurs around 1 year of age, and that the light-colored is possible that the gonads of S. griseus develop and rest band forms around October; however, this trend might during the periods of rising and declining water temperature, vary across individuals. The dark and light bands that form respectively. alternately in the ossicles of sea urchins are due to changes A similar phenomenon was reported for M. quinquies- in density when the calcareous component is deposited perforata, whereby the gonads developed from the growth (Gage and Tyler 1985; Sano et al. 2001). Such changes stage to the spent stage between spring and summer, when in the density of calcareous deposits might be caused the water temperature rose, and then shifted to the rest- by periodic changes in physiological factors, includ- ing stage from fall to winter, when the water temperature ing metabolism and reproduction (Gage and Tyler 1985; dropped (Tavares and Borzone 2006). Reports of closely Sano et al. 2001), as well as environmental factors, such

Table 2 Population density, Stn. 1 Stn. 2 Stn. 3 Stn. 4 Stn. 5 Mean SD mean, maximum and minimum test diameter of S. griseus at Density (ind./m2) 220 218 199 190 257 216.8 25.8 5-m depth of Motomachi, Mean test diameter (mm) 40.3 40.7 40.8 39.0 40.9 40.3 0.8 Tomakomai, Japan Maximum test diameter (mm) 51.8 51.4 47.9 47.4 50.8 49.9 2.1 Minimum test diameter (mm) 12.3 10.7 16.6 10.0 29.2 15.8 7.9

Stn. Station, ind. individuals

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20 107.5 mm at 3 years of age (Lane and Lawrence 1980). Fur- A. manni C) thermore, individuals of up to 9 years of age were (° 15 collected of the coast of Jeju Island, South Korea, with test diameters at 1, 2, 3, 5, 7, and 9 years of age of 51.4, 83.7, 10 102.7, 126.5, 142.2, and 153.9 mm, respectively (Kang et al. 2007). In comparison to these three sand dollar populations, S. griseus 5 the population in Tomakomai had the smallest maximum test diameters, even though it exhibited the char- Water temperature acteristic rapid growth at a young age. Furthermore, the life 0 Dec Jan Feb Mar Apr May JunJul AugSep OctNov span of S. griseus in Tomakomai was shorter than that of Month (2016-2017) other sand dollar populations: the life spans of excentricus, which belongs to the family Dendrasteridae, and Echinarachnius parma Fig. 9 Monthly change in mean water temperature from December , which belongs to the family Echi- 2016 to November 2017 narachniidae, have been reported to be about 8 years (Birke- land and Chia 1971; Steimle 1989). In addition, rapid growth at a young age, which is common in sand dollars, might as water temperature and feeding conditions (Pearse and reduce the risk of predation, enhance their competitiveness Pearse 1975; Duineveld and Jenness 1984; Ebert and Rus- in acquiring food (i.e., organic sediments), and increase their sell 1988; Gage 1991). Thus, the dark band of S. griseus physical stability against waves and tidal currents. might be formed in 1-year cycles because the density of There is concern among fshermen in Hokkaido that the calcareous components deposited on the interambulacral fshing grounds of P. sachalinense are being reduced due plate decreases due to high water temperature in summer to the dense distribution of S. griseus. Therefore, we quan- or because of the physiological changes associated with titatively surveyed the population density of S. griseus in breeding. In addition, individuals with dark bands that Tomakomai at a water depth of 5 m, where the sand dollars formed around the outer edge of the interambulacral plate are distributed particularly densely (Sakurai et al. 1991). were observed throughout the survey period of this study. Sand dollars with an average test diameter of 39.0–40.9 mm This phenomenon indicates that the dark band continues were distributed at a density of 190–257 individuals/m2. In to form in some individuals in the absence of light bands, comparison, S. griseus was distributed at a maximum of even after the dark band appeared in June–July, due to 220 individuals/m2 on a sunray surf clam Mactra chinensis factors other than high water temperature and breeding. bed in Shimamaki, Hokkaido (Sakurai et al. 2001), and a To clarify the relationship between the age and growth of maximum of 1,000 individuals/m2 on a P. sachalinense bed S. griseus in this study, we assigned age and test diameter in Yoichi, Hokkaido (Sakurai et al. 2003). Thus, S. griseus to von Bertalanfy, Gompertz and logistic curves and esti- is distributed at almost the same density in Tomakomai as mated the parameters of each curve by the maximum likeli- in Shimamaki. However, D. excentricus might exclude sev- hood method. The age of each specimen was in the range of eral tube-building crustaceans (Smith 1981) and Leptochelia 1–6 years, with a maximum test diameter of 46.8 mm. The dubia of the order Tanaidacea (Highsmith 1982) from their Gompertz curve with the smallest AIC value had the best ft habitats due to their dense distributions. Because S. griseus among the three curves. The test diameter at each age based might inhibit the recruitment of P. sachalinense by causing on the obtained Gompertz curve was calculated as 9.0 mm bioturbation through burrowing and feeding (Hayashi et al. at 1 year, 20.7 mm at 2 years, 30.3 mm at 3 years, 36.3 mm 1963; Sakurai et al. 2003), it is necessary to clarify the pres- at 4 years, 39.4 mm at 5 years and 40.9 mm at 6 years of age. ence of interspecifc relationships and the current situation In addition, it was inferred that the growth rate of S. griseus regarding the habitat of the two species in question. in Tomakomai reaches its maximum at 1.6 years of age, after This study indicates that S. griseus in Tomakomai over which growth slows until a theoretical maximum is reached the age of 3 years with a test diameter of > 30 mm, which at a test diameter of 42.3 mm. currently account for a large proportion of the population, In comparison, S. mirabilis in Vostok Bay, Russia, on should be removed prior to the start of the spawning season the coast of the Sea of Japan had an estimated test diameter in June. This approach would provide a way of efciently of 23.4, 32.6, and 44.0 mm at 1 year, 2 years and 3 years of reducing the density of the sand dollar population, as well age, respectively (Brykov and Parasyna 1978). Ten-year-old as preventing the establishment of juveniles. It was not individuals with a test diameter exceeding 60.0 mm were possible to verify the size at sexual maturity of S. griseus also caught in small numbers (Brykov and Parasyna 1978). because we could not collect enough small specimens con- The test diameter of M. quinquiesperforata in Tampa Bay, tinuously. To exterminate the sand dollar, individuals with a Florida was 46.5 mm at 1 year, 72.0 mm at 2 years, and size that exceeds that at sexual maturity should be targeted.

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Therefore, it is necessary to undertake further studies to age Creed EL, Coull BC (1984) Sand dollar, Mellita quinquiesperforata Renilla reniformis small specimens of the sand dollar by gonadal observation (Leske), and sea pansy, (Cuvier) efects on meiofaunal abundance. J Exp Mar Biol Ecol 84:225–234 and to clarify the size at which sexual maturity is reached. Drozdov AL, Vinnikova VV (2010) Morphology of gametes in sea Reidenauer (1989) showed that a density of 12 individu- urchins from Peter the Great Bay, Sea of Japan. Russ J Dev als/m2 M. quinquiesperforata disturbed about 0.14 m2 of Biol 41:37–45 sediment surface per hour (i.e. 1 individual disturbs 0.28 m2/ Duineveld GCA, Jenness MI (1984) Diferences in growth rates of the Echinocardium cordatum as estimated by the day) by its burrowing action, which decreased the abundance parameter w of the von Bertalanfy equation applied to skeletal of meiofauna, including harpacticoid species, Halectino- rings. Mar Ecol Prog Ser 19:65–72 soma sp., and mites. Yeo et al. (2013) showed that Peronella Ebert TA, Russell MP (1988) Latitudinal variation in size structure lesueuri (family Laganidae) randomly moved at a rate of of the west coast purple sea urchin: a correlation with head- lands. Limnol Oceanogr 33:286–294 3.9–5.3 cm/h in the summer and 2.0–2.7 cm/h in the winter, Findley RH, White DC (1983) The efects of feeding by the sand dol- and estimated that one of these sand dollars may biotur- lar Mellita quinquiesperforata (Laske) on the benthic microbial bate a sediment surface of about 0.1 m2/day. Although the community. J Exp Mar Biol Ecol 72:25–41 degree of burrowing action and bioturbation by S. griseus Gage JD (1991) Skeletal growth zones as age-markers in the sea urchin Psammechinus miliaris. Mar Biol 110:217–228 is not known, if this species has the same burrowing and Gage JD, Tyler PA (1985) Growth and recruitment of the deep-sea movement ability as M. quinquiesperforata and P. lesueuri, urchin Echinus afnis. Mar Biol 90:41–53 it is estimated that S. griseus inhabiting an area of 1 m2 Gorie S (2001) Estimation of the parameters in von Bertalanfy’s could bioturbate sediment surfaces of 53.2–72.0 m2, which growth formula by MS-Excel. Aquac Sci 49:519–527 (in Japa- 2 nese with English abstract) is equivalent to 19.0–25.7 m /day. Furthermore, Li et al. Hayashi T (1988) Occurrence, distribution and mortality of juvenile (2013) showed that bioturbation by P. lesueuri decreases surf clam, Pseudocardium sybillae (Valenciennes), in natural the photosynthetic rate of benthic microalgae. In addition, beds. Fish Eng 24:45–52 (in Japanese with English abstract) bioturbation caused by the feeding and movement of Encope Hayashi T, Kawamura K, Saito K, Terai K, Wakui T (1962) About emarginata Japanese surf clam. Part 1. J Hokkaido Fish Exp St 19:538–548 (family Mellitidae) infuences the structure of (in Japanese) microphytobenthic assemblages (Brustolin et al. 2016). P. Hayashi T, Kawamura K, Saito K, Terai K, Wakui T (1963) About sachalinense mainly feeds on benthic diatoms that belong Japanese surf clam. Part 2. J Hokkaido Fish Exp St 20:16–28 to the orders Pennales and Centrales (Ohashi et al. 2014). (in Japanese) S. griseus Hayashi T, Terai K, Arima K (1967) Studies on the planktonic larvae Thus, assuming that disturbs the sediment surface and young shells of Japanese surf clam, Spisula sachalinensis of the study area, bioturbation likely infuences the feeding Schrenck, on the coast of Yakumo, Oshima Prov., Hokkaido. Sci environment of the surf clam. Therefore, it is necessary to Rep Hokkaido Fish Exp Stn 7:8–71 (in Japanese with English clarify how the burrowing, movement, and feeding activity abstract) S. griseus Highsmith RC (1982) Induced settlement and metamorphosis of sand of afect the benthic community, including benthic dollar () larvae in predator-free sites: diatoms. adult sand dollar beds. Ecology 63:329–337 Jensen M (1969) Age determinations of echinoids. Sarsia 37:41–44 Acknowledgements We thank Mr. K. Akazawa (Tomakomai Fisheries Kang DH, Yang HS, Park HS, Choi KS (2007) Use of plate growth Cooperative Association), Mr. N. Makiguchi, Ms. S. Iimura, and Mr. measurement for the estimation of skeletal growth of two sand H. Ikarashi (Hokkaido Aquaculture Promotion Corporation), Mr. T. dollars, Astriclypeus manni (Verrill 1867) and Clypeaster Iwamoto and Mr. H. Fukui (Tokai University) for assisting in this work. japonicus (Döderlein 1885), in Jeju, Korea. 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