Density, Growth and Reproduction of the Sea Urchin Anthocidaris Crassispina (A

Blackwell Science, LtdOxford, UK FISFisheries Science0919-92682004 Blackwell Science Asia Pty Ltd 702April 2004 796 Sea urchin density, growth and reproduction K Yatsuya and H Nakahara 10.1046/j.1444-2906.2003.00796.x Original Article233240BEES SGML

FISHERIES SCIENCE 2004; 70: 233–240

Density, growth and reproduction of the sea urchin Anthocidaris crassispina (A. Agassiz) in two different adjacent habitats, the Sargassum area and Corallina area

Kousuke YATSUYAa* AND Hiroyuki NAKAHARA

Graduate School of Global Environmental Studies, Kyoto University, Kyoto, Kyoto 606-8501, Japan

ABSTRACT: The sea urchin Anthocidaris crassispina (A. Agassiz) is a dominant herbivore on rocky shores in the warm temperate region of Japan. To clarify the relationship between macroalgal community and A. crassispina on rocky shores, A. crassispina collected in the Sargassum area and neighboring Corallina area were compared with respect to their density, growth and reproduction. Density of A. crassispina was higher in the Corallina area than in the Sargassum area. A. crassispina in the Sargassum area reached a larger size and had higher gonad indices than those in the Corallina area throughout the year. The annual reproductive cycles were almost the same in the two different habitats. These results indicate that Sargassum spp. support better growth and reproduction of A. crassispina.

KEY WORDS: Anthocidaris crassispina, articulated coralline turf, Corallina, density, growth, reproduction, Sargassum, Sargassum forest.

INTRODUCTION Reproduction of the sea urchin has been well studied throughout the world because of the Much attention has been given to the interactions commercial value of the gonad.10,11 Anthocidaris between sea urchin and seaweed. The impor- crassispina is an edible sea urchin and has com- tance of sea urchins in structuring macroalgal mercial value.12 The annual reproductive cycle of communities is well known.1–3 Macroalgal com- A. crassispina was investigated in Southern munities can affect the growth and reproduction Korea,13 Hong Kong14 and Japan.15–18. In some spe- of sea urchins.4–6 These interactions have been cies of sea urchins, differences in the reproduc- studied mostly on kelp forest. tive maturation between differing habitats have In the middle part of the Japan Sea coast of Hon- been studied,10,19,20 but for A. crassispina the shu, Sargassum species, rather than kelp species, effects of habitat on reproduction have not been form dense forests. Sea urchin Anthocidaris cras- examined. sispina (A. Agassiz) is one of the dominant benthic The purpose of the present study was to clarify herbivores in this region.7 However, little is known the differences in density, growth, and reproduc- of the effects of A. crassispina on macroalgal tion of A. crassispina in two different adjacent communities.8 macroalgal communities, Sargassum forest and In some rocky shores of Japan, sea urchin- articulated coralline turf. dominated encrusting coralline ﬂats appear in the deeper area of the macroalgal forests.9 The ecology of sea urchins in these habitats has been docu- MATERIALS AND METHODS mented.6 But sea urchins in articulated coralline turf, located in shallow area (<2 m in depth), have Study site not been investigated. The study site is located in Kodomari (35∞32¢N; 135∞31¢E), a small bay open to the north-east, in *Corresponding author: Tel: 81-75-753-6356. Fax: 81-75-753-6375. Email: [email protected] the western part of Wakasa Bay, central part of aPresent address: Kyoto Institute of Oceanic and Fishery Japan Sea coast (Fig. 1). At this site, the Sargas- Science, Miyazu, Kyoto 626-0052, Japan. sum forest extends to approximately 12 m in Received 30 April 2003. Accepted 6 November 2003. depth. However, in some shallow parts of the

234 FISHERIES SCIENCE K Yatsuya and H Nakahara

Fig. 1 Map of the study site. The area indicated by dashed lines is the Sargassum area and the area enclosed by dotted lines is the Corallina area. Transect lines 1 and 2 are in the Sargassum area and 3 and 4 are in the Corallina area, respectively.

subtidal zone (<1.2 m in depth), articulated cor- packed with one A. crassispina. The Corallina alline algae, rather than Sargassum, dominate. area is more wave-exposed than the Sargassum The sea urchin A. crassispina can be observed in area because of the topographical features; the both areas. Hereafter, we refer to these habitats water in the Corallina area is shallower and as the Sargassum area and Corallina area, there is a steep depth gradient bordering this because of the domination of Sargassum spp. area. and Corallina pilulifera Postels et Ruprecht, respectively. In the shallow subtidal Sargassum area next to Abundance of seaweed the Corallina area, two transect lines (lines 1 and 2) were installed perpendicular to the shoreline Biomass and percentage cover in the two habitats (Fig. 1). These lines were 20 m long and at a depth in the same depth range, were estimated by of 0.3–1.8 m. The substratum was gently sloping monthly sampling from October 1998 to November and consisted of rock and medium- to large-sized 1999. Four quadrates (25 ¥ 50 cm2) in the Sargas- boulders (approx. 0.5–3.0 m in the largest dimen- sum area and three (50 ¥ 50 cm2) in the Corallina sion). The urchin A. crassispina in this area inhab- area were placed along one transect line at 5 m ited the crevices in rocks and the undersides of intervals to represent the vegetation of the two boulders. areas. Transect line 2 in the Sargassum area and In the Corallina area, two transect lines (lines transect line 4 in the Corallina area were investi- 3 and 4) were installed perpendicular to the gated. Erect seaweed larger than 3 cm in the quad- shoreline (Fig. 1). These lines were 15 m long rates were taken to the laboratory, then sorted and and at a depth of 0.3–1.2 m. The substratum was wet-weighed. For seaweed smaller than 3 cm, the gently sloping ﬂatrock. Anthocidaris crassispina percentage cover was calculated in the same quad- in this area lived in holes in the ﬂatrock. These rates. All seaweed samples were added together, holes were approximately 10 cm deep and 10– and then biomass and percentage cover in two 15 cm in diameter and each hole was tightly areas were estimated.

Sea urchin density, growth and reproduction FISHERIES SCIENCE 235

Density and size of Anthocidaris crassispina (a)

The density and size of A. crassispina was estimated by monthly investigation from October 1998 to September 1999. Anthocidaris crassispina inhabiting both sides within 0.75 m of the two transect lines in each habitat, were counted, and A. crassispina under boulders or in crevices were carefully searched for to obtain precise estimates. Ten to 25 A. crassispina that were located away from the transect lines were randomly collected from each habitat. They were transferred to the laboratory, the horizontal test diameter was measured with vernier calipers to the nearest millime- ter, and the wet weight was measured to the nearest 0.1 g. (b)

Growth of Anthocidaris crassispina

Rings in interambulacral plates were counted to Fig. 2 Sketch of the interanmbulacral plate showing determine the age of A. crassispina. Twelve urchins annual rings ground (a) horizontally and (b) vertically. from each habitat were collected on 9 December This figure shows four rings. 1999. The horizontal test diameters of these urchins were 47–67 mm in the Sargassum area and the gonad (7 mm) were stained with Mayer’s hema- 20–50 mm in the Corallina area, respectively. The toxylin and eosin. The reproductive maturation of following procedure was performed according to 21 A. crassispina were classified according to the five Pearse and Pearse with some modification maturation stages used by previous authors:15,23 (heated in an oven at 300∞C for 5 h). To obtain stage 1, recovering; stage 2, growing; stage 3, clearer results we ground the plate vertically and premature; stage 4, mature; and stage 5, spent. horizontally (Fig. 2). Rings in the plates were counted under the microscope. The number of rings in the plate varied with the Migration of Anthocidaris crassispina location of the plate, because new plates emerged 21 as it grew and plates near the oral and aboral To examine the migration, A. crassispina were region were so small that rings in those plates were removed from an area measuring 1 m2 in the Cor- 21 fused. The maximum number of rings was allina area at the end of September 1999. Observa- regarded as the age of A. crassispina. tions were carried out until the end of December 1999, to see whether A. crassispina entered that area. In the Sargssum area, the monthly observa- Reproduction of Anthocidaris crassispina tions along the transect lines make it possible to confirm the location of A. crassispina. The monthly collected A. crassispina, measured for size and weight, were dissected for gonad observa- tion. The gonads were placed on a paper towel to Density of starfish remove excess water and wet-weighed to the nearest 0.1 g. The gonad index (GI) was expressed as In the present study site, Asterina pectinifera Mül- GI = [(weight of gonad)/(total body weight)] ¥ 100. laer and Troschel was the most prominent predator on sea urchins. Asterina pectinifera were distrib- Because small, immature sea urchins have uted in both areas. The other predators were unproportionally small gonads,15,22 A. crassispina not easily observed. The density of starfish >40 mm in test diameter were used for calculating A. pectinifera was also estimated on 27 December gonad indices. 1999. The starfish between the two transect lines in All collected A. crassispina were included in the each area were counted. Those areas measured histological studies. A piece of the gonad was fixed 135 m2 and 69 m2 in the Sargassum area and Coral- overnight in Bouin’s solution. Paraffin sections of lina area, respectively. 236 FISHERIES SCIENCE K Yatsuya and H Nakahara

RESULTS over 55.6–64.6 mm and 40.9–48.4 mm in the Sargassum and Corrallina area, respectively Biomass and percentage cover of seaweed (Table 1). Monthly mean wet weight ranged from 90.0–128.6 g and 38.8–60.5 g in the Sargassum The dominant seaweed species in the Sargassum area and Corallina area, respectively (Table 1). area were Myagropsis myagroides (Turner) Fen- The density of A. crassispina, estimated monthly, sholt, Sargassum patens C. Agardh, and Sargassum in the Corallina area was two orders of magni- piluliferum C. Agardh. In the Corallina area, Coral- tude higher than in the Sargassum area. Mean lina pilulifera and Amphiroa spp. dominated and and standard deviation of A. crassispina density Sargassum spp. were scarce. was 11.1 ± 3.4 and 0.3 ± 0.1 urchins/m2 in the The biomass of seaweed was significantly differ- Corallina area and Sargassum area, respectively ent between the two habitats (Fig. 3). In the Sargas- (Table 1). sum area it was more than 2.5 kg/m2 throughout the year and in the Corallina area it was consis- tently below 1.0 kg/m2. The biomass of seaweed in Growth of Anthocidaris crassispina the Sargassum area continued to increase through autumn and winter, and reached the highest value Figure 4 shows the relationship between test diam- (21.2 kg/m2) in March. Then it decreased to its low- eter and the number of rings in the interambulac- est (2.5 kg/m2) in July. In the Corallina area ral plate. Specimens of A. crassispina collected in seaweed biomass ranged from 22.4 to 718.3 g/m2. the Sargassum area had larger test diameter than Percentage covers of understory species were those with the same number of rings in the Coral- also different. In the Sargassum area, encrusting lina area. The A. crassispina specimens collected in coralline algae and Gelidium spp. were promi- the Sargassum area had significantly more rings nent. In the Corallina area Corallina pilulifera was than those in the Corallina area (t-test, P < 0.05). the most dominant and the percentage cover of The A. crassispina specimens collected in the articulated coralline algae in this area was >80%, except for May to August 1999, when it was 50–60%. The other components of the algal cover Table 1 Anthocidaris crassispina density, size, gonad were Dictyopteris prilifera (Okamura) Okamura, and predator density Dictyota dicotoma (Hudson) Lamouroux, Cla- Sargassum Corallina dophora spp., Hypnea spp. and encrusting coral- area area line algae. Drift algae (detached macroalgae lying on the Density (ind./m2) 0.31 ± 0.11 11.10 ± 3.37 bottom) were observed only in the Sargassum area Test diameter (mm) 55.6 – 64.6 40.9 – 48.4 in May–June 1999. Wet weight (g) 90.0 – 128.6 38.8 – 60.5 Biomass (g wet wt/m2) 20.0 – 74.3 299.8 – 854.2 Gonad index 8.4 ± 2.3 6.2 ± 2.1 2 Size, weight, and density of Starfish density (ind./m ) 0.0043 0.20 Anthocidaris crassispina Density and gonad index are expressed as mean ± SD of monthly mean (n = 12), and test diameter, wet weight and Anthocidaris crassispina in the Sargassum area biomass are expressed as the range of monthly mean (n = 12). were larger than in the Corallina area throughout the year. Monthly mean test diameter ranged

Fig. 4 Relationship between the number of rings and Fig. 3 Seasonal changes in seaweed biomass in the () test diameter of Anthocidaris crassispina in the () Sargassum area and () Corallina area. Sargassum area and (▲) Corallina area. Sea urchin density, growth and reproduction FISHERIES SCIENCE 237

Sargassum area might have had a higher growth July). No migration of A. crassispina was observed rate and longer lifespan. in either habitat.

Starfish density Reproduction of Anthocidaris crassispina The density of the starfish A. pectinifera was much The seasonal changes in monthly mean gonad higher in the Sargassum area (0.20 individuals/m2) indices of A. crassispina collected from the two than the Corallina area (0.0043 individuals/m2; different habitats are given in Fig. 5. The monthly Table 1). Radius of the A. pectinifera ranged from 3 mean gonad indices were significantly higher in to 5 cm in both habitats. the Sargassum area than those in the Corallina area (ANOVA P < 0.001; Fig. 5). The gonad index in the Sargassum area increased gradually from DISCUSSION October 1998 to May 1999, and reached 11.8 at the peak value. Then it decreased to 3.6 in Sep- Anthocidaris crassispina densities in the two tember. The same pattern of fluctuation was neighboring habitats were considerably different. observed in the Corallina area. It increased to a In the Corallina area it was 11.1 ± 3.4 urchins/m2 peak value of 9.0 in June and decreased to 3.4 in and in the Sargassum area it was September. The decrease in the gonad index 0.3 ± 0.1 urchins/m2. The sea urchin density may after spawning season, represented by the maxi- change in response to predation and migration. mum minus the minimum gonad index, was 8.2 Predators of sea urchins include starfish,24,25 rock in the Sargassum area and 5.6 in the Corallina area. Few differences were found in the annual gametogenic cycle in the two different habitats, except for a prolonged spent stage for male specimens in the Corallina area (Fig. 6). This figure shows that gonad maturation started in autumn to winter and spawning commenced in June and continued to September in both habitats.

Migration of Anthocidaris crassispina

The Corallina area was observed for 3 months to see if sea urchins entered this sea urchin-empty area, and this did not happen during that time. In the Sargassum area, the sea urchin locations were investigated monthly; it was conﬁrmed that almost all of the sea urchins did not migrate because each sea urchin was located at the same position at two successive times (e.g. June and

Fig. 5 Seasonal changes in gonad index of Anthocidaris crassispina in the () Sargassum area and () Corallina area. The symbols and error bars indicate monthly mean Fig. 6 Gametogenic cycles in Anthocidaris crassispina and SD, respectively. in the Sargassum area and Corallina area. 238 FISHERIES SCIENCE K Yatsuya and H Nakahara

crab,26,27 lobsters,28 sea otters,29 and sheephead.30 droebachiensis.20,32 These studies revealed that In the present study site starfish A. pectinifera was kelp supports better gonad growth than calcare- observed. Asterina pectinifera preys on the sea ous algae. Although Sargassum confusum C. urchin Hemicentrtotus pulcherrimus,25 younger Agardh was reported to be less nutritious than (1–2 cm) Strongylocentrotus nudus26 and Strongy- kelp for Strongylocentrotus nudus,36 Sargassum locentrotus intermedius seedlings.27 The density of spp. might also support gonad growth of starfish in the Sargassum area was 50-fold A. crassispina.34 higher than that in the Corallina area. A lower Anthocidaris crassispina in Wakasa Bay, the A. crassispina density in the Sargassum area Japan Sea, was examined in terms of gonad index might be partly attributed to predation by star- and spawning period37 but not in terms of histolog- fish. Migration of A. crassispina might not change ical studies. Histological studies would offer more the density because migration of A. crassispina detailed information on the reproductive cycle, has never been observed at this site at least in and enable comparisons of the reproductive cycle autumn. biogeographically. The reproductive cycles were Maturation of gonad simultaneously started in almost synchronous between the two different two habitats (Fig. 6). Anthocidaris crassispina in habitats. This synchrony in the annual reproduc- both habitats might recruit at the same time tive cycles may be controlled by water tempera- and it is possible to compare the growth rate of ture.38 Anthocidaris crassispina did not mature at A. crassispina between the two habitats. 15∞C but matured at 20∞C and 25∞C.38 The popula- Anthocidaris crassispina specimens in the Sar- tions of A. crassispina in the Izu Peninsula, on the gassum area grew to 46.2 mm in test diameter in central part of the Pacific coast of Japan16 and in 2 years, and in the Corallina area the urchins the Hirado Island, at the eastern end of the East reached 33.0 mm in 2 years. The growth rate of China Sea,15 have prolonged spawning periods. A. crassispina around the Miura Peninsula, on the Mature gonads in A. crassispina appeared from central part of the Pacific coast of Japan, was May to August in the Izu Peninsula and from June reported to be 32.0 mm in 2 years.12 In Hokkaido, to September in the Hirado Island. At the present in the northern part of Japan, Strongylocentrotus study site in Wakasa Bay, mature gonads appeared intermedius reached 23.7 mm5 and Strongylocen- in July and August. The water temperature might trotus nudus reached 38.4 mm in 2 years,6 respec- have an effect on spawning period. tively. Anthocidaris crassispina in the Sargassum The density and size of A. crassispina differed area grows faster than the same species in other between the two habitats. There were large num- habitats and the two Strongylocentrotus species in bers of small sea urchins crowded into the Coral- Hokkaido. lina area and small numbers of large sea urchins in The effects of habitat on the growth rate of sea the Sargassum area. One explanation for this urchins have been well documented and research- difference might be that the Corallina area is an ers have been interested in food availability5,31–33 unfavorable habitat for the growth and gonad and spine abrasion.31 In the present study, development of adult A. crassispina but a favorable A. crassispina in the Sargassum area fed mainly on one for young urchin for the following reasons: (i) Sargassum spp. while those in the Corallina area articulated coralline algae might provide a refuge fed less on Sargassum spp. and more on calcareous from predators;39 (ii) there are fewer predations on algae.34 Sargassum spp., which are more nutritional the young urchins; (iii) detritus and/or microalgae, than calcareous algae, would lead to the higher which constitute the diet of young urchins,4 are growth rate in the Sargassum area. The wave action more abundant in the Corallina area; (iv) plank- strength was different between the two habitats. tonic A. crassispina larvae are prone to settle in the Stronger wave action in the Corallina area might Corallina area; and (v) many holes in flat rocks pro- induce spine abrasion, requiring more energy for vide refuge for urchins against predators and wave repair and thus suppressing growth rate.31 Strong exposure. If so, the Corallina area would be a wave action might dislodge urchins and prevent suitable habitat for young urchins and the urchin them from feeding.35 density would be high. The gonad indices were generally higher in the In the next step, studies on the factors regulating Sargassum area than in the Corallina area. Food A. crassispina density in relation to the macroalgal availability might contribute to the fluctuations of communities should be carried out. These factors the gonad indices. Previous studies examined the might relate to early life-history parameters (e.g. effect of food availability on the gonad indices of mortality of planktonic larva, success in recruit- the sea urchins, Evechinus chloroticus,19 Strongy- ment into the benthic stage, and survival of juve- locentrotus intermedius,5 Paracentrotus lividus,10 niles). The early life-history of A. crassispina in Strongylocentrotus nudus6 and Strongylocentrotus different habitats is still not understood. Sea urchin density, growth and reproduction FISHERIES SCIENCE 239

ACKNOWLEDGMENTS Mladevov PV, Lambert P, Parsley RL (eds). Echinoderm Biology. Balkema, Rotterdam. 1988; 193–204. We are grateful Dr Masahiro Ueno, Fishery 15. Yamazaki M, Kiyomoto S. Reproductive cycle of the sea Research Station, Kyoto University, for valuable urchin Anthocidaris crassispina from Hirado Island, Nagasaki Prefecture. Bull. Seikai Natl Fish. Res. Inst. 1993; advice on field survey. We would also like to thank 71: 33–40. the librarians of the Graduate School of Agricul- 16. Horii T. The annual reproductive cycle and lunar spawning ture, Kyoto University, for collecting scientific rhythms of the purple sea urchin Anthocidaris crassispina. papers. This is contribution no.143 from Kyoto Nippon Suisan Gakkaishi 1997; 63: 17–22. Institute of Oceanic and Fishery Science. 17. Masuda R, Dan JC. Studies on the annual reproductive cycle of the sea urchin and the acid phosphatase activity of relict REFERENCES ova. Biol. Bull. 1977; 153: 577–590. 18. Sano M. Annual life cycles of sea urchins on rocky shore in Awashima, Niigata Prefecture. In: Proceedings of Japan 1. Lawrence JM. On the relationships between marine plants Sea Block Zouyousyoku Kenkyu Suisin Renraku Kaigi. and sea urchins. Oceanogr. Mar. Biol. Ann. Rev. 1975; 13: Japan Sea National Fisheries Research Institute, Niigata. 213–286. 2003; 3–4. 2. Harrold C, Pearse JS. The ecological role of echinoderms in 19. Dix TG. Biology of Evechinus chloroticus (Echinoidea: Echi- kelp forests. Echinoderm Stud. 1987; 2: 137–233. nometridae) from different localities III. Reproduction. N.Z. 3. Elner RW, Vadas RL. Inference in ecology: the sea urchin J. Mar. Freshw. Res. 1970; 4: 385–405. phenomenon in the northwestern Atlantic. Am. Nat. 1990; 20. Meidel SK, Scheibling RE. Annual reproductive cycle of the 136: 108–125. green sea urchin, Strongylocentrotus droebachiensis, in dif- 4. Fuji A. Ecological studies of the growth and food consump- fering habitats in Nova Scotia, Canada. Mar. Biol. 1998; 131: tion on Japanese common littoral sea urchin, Strongylocen- 461–478. trotus intermedius (A. Agassiz). Mem. Fac. Fish. Hokkaido 21. Pearse JS, Pearse VB. Growth zones in the echinoid skeleton. Univ. 1967; 15: 83–160. Am. Zool. 1975; 15: 731–753. 5. Kawamura K. Fishery biological studies on a sea urchin, 22. Gonor JJ. Gonad growth in the sea urchin, Strongylocentro- Strongylocentrotus intermedius (A. Agassiz). Sci. Rep. tus purpuratus (Stimpson) (Echinodermata: Echinoidea) Hokkaido Fish. Exp. Stn 1973; 16: 1–54. and the assumptions of gonad index methods. J. Exp. Mar. 6. Agatsuma Y. Ecological studies on the population dynamics Biol. Ecol. 1972; 10: 89–103. of the sea urchin Strongylocentrotus nudus. Sci. Rep. 23. Fuji A. Studies on the biology of the sea urchin I. Super- Hokkaido Fish. Exp. Stn 1997; 51: 1–66. ficial and histological gonadal changes in gametogenic 7. Hayashi I, Konno T, Yamakawa H. Distributional character- process of two sea urchins, Strongylocentrotus nudus and istics of benthic organisms in shallow sublittoral rocky areas S. intermedius. Bull. Fac. Fish. Hokkaido Univ. 1960; 6: 1– of Mikuni, Fukui Prefecture: Part of the survey on the effects 14. of the Nakhodka oil spill. Bull. Jpn Sea Natl Fish. Res. Inst. 24. Duggins DO. Starfish predation and the creation of mosaic 2000; 50: 43–137. patterns in a kelp-dominated community. Ecology 1983; 64: 8. Yotsui T, Maesako N. Restoration experiments of Eisenia 1610–1619. bycyclis beds on barren grounds at Tsushima Islands. 25. Kurihara T. Studies on changes in Asteroidea distribution Suisanzoshoku 1993; 41: 67–70. due to prey organisms. PhD Thesis. Kyoto University, Kyoto, 9. Sano M, Omori M, Taniguchi K, Seki T. Life cycle of the sea Japan, 1999. urchin Strongylocentrotus nudus with growth and matura- 26. Shiraishi K. Effect of water temperature on the predation of tion in relation to marine algal zonation in an infralittoral the sea urchin, Strongylocentrotus nudus. Suisanzoshoku zone. In: Taniguchi K (ed). The Ecological Mechanism of 1997; 45: 321–325. ‘Isoyake’ and Marine Afforestation. Kouseisha Kouseikaku, 27. Kawai T, Agatsuma Y. Predators on released seed of the sea Tokyo. 1999; 73–83. urchin Strongylocentrotus intermedius at Shiribeshi, 10. Byrne M. Annual reproductive cycles of the commercial sea Hokkaido, Japan. Fish. Sci. 1996; 62: 317–318. urchin Paracetrotus lividus from an exposed intertidal and 28. Breen PA, Mann KH. Changing lobster abundance and the a sheltered habitat on the west coast Ireland. Mar. Biol. destruction of kelp beds by sea urchin. Mar. Biol. 1976; 34: 1990; 104: 275–589. 137–142. 11. King CK, Hoegh-Guldberg O, Byrne M. Reproductive cycle 29. Estes JA, Smith NS, Palmisano JF. Sea otter predation and of Centrostephanus rodgersii (Echinoidea), with recommen- community organization in the western Aleutian Island, dations for the establishment of sea urchin fishery in New Alaska. Ecology 1978; 59: 822–833. South Wales. Mar. Biol. 1994; 120: 95–106. 30. Cowen RK. The effect of sheephead (Semicossyphus pul- 12. Imai T. Studies on the sea urchin propagation in central cher) predation on red sea urchin (Strongylocentrotus Japan. Special Rep. Kanagawa Pref. Fish. Exp. Stn 1995; 6: 1– franciscanus) population: An experimental analysis. 90. Oecologia 1983; 58: 249–255. 13. Yoo SK, Hur SB, Ryu HY. Growth and spawning of the sea 31. Ebert TA. Growth rates of the sea urchin Strongylocentrotus urchin Anthocidaris crassispina (A. Agassiz). Bull. Korean purpuratus related to food availability and spine abrasion. Fish. Soc. 1982; 15: 345–358. Ecology 1968; 49: 1075–1091. 14. Chiu ST. Reproductive biology of Anthocidaris crassispina 32. Vadas RL. Preferential feeding: An optimization strategy in (Echinodermata: Echinoidea) in Hong Kong. In: Burke RD, sea urchins. Ecol. Monogr. 1977; 47: 337–371. 240 FISHERIES SCIENCE K Yatsuya and H Nakahara

33. Larson BR, Vadas RL, Keser M. Feeding and nutritional ecol- urchin, Strongylocentrotus nudus. Sci. Rep. Hokkaido Fish. ogy of the sea urchin Strongylocentrotus droebachiensis in Exp. Stn 1999; 54: 33–40. Maine, USA. Mar. Biol. 1980; 59: 49–62. 37. Tsuji S, Yoshiya M, Tanaka M, Kuwahara A, Uchino K. Sea- 34. Yatsuya K, Nakahara H. Diet and stable isotope ratios of sonal changes in distributions and ripeness of gonad of a gut contents and gonad of sea urchin, Anthocidaris cras- sea urchin Strongylocentrotus nudus in the western part of sispina (A. Agassiz) in two different adjacent habitats, Wakasa Bay. Bull. Kyoto Inst. Oceanogr. Fish. Sci. 1989; 12: Sargassum area and Corallina area. Fish. Sci. 2004; 70: 15–21. 285–292. 38. Sakairi K, Yamamoto M, Ohtsu K, Yoshida M. Environmen- 35. Kawamata S. Effects of wave-induced oscillatory ﬂow on tal control of gonadal maturation in laboratory-reared sea grazing by a subtidal sea urchin Strongylocentrotus urchins, Anthocidaris crassispina and Hemicentrotus nudus (A. Agassiz). J. Exp. Mar. Biol. Ecol. 1998; 224: 31– pulcherrimus. Zool. Sci. 1989; 6: 721–730. 48. 39. Akioka H, Baba M, Masaki T, Johansen HW. Rocky shore 36. Nabata S, Hoshikawa H, Sakai Y, Funaoka T, Oohori T, Ima- turfs dominated by Corallina (Corallinales, Rhodophyta) in mura T. Food value of several algae for growth of the sea northern Japan. Phycol. Res. 1999; 47: 199–206.