Fisheries Science (2019) 85:465–474 https://doi.org/10.1007/s12562-019-01297-0 ORIGINAL ARTICLE Biology Reproductive cycle and growth of the sand dollar 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 Vol.:(0123456789)1 3 466 Fisheries Science (2019) 85:465–474 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. 1 3 Fisheries Science (2019) 85:465–474 467 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.