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 esti- mated 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 mea- sured 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 2 region were so small that rings in those plates were removed from an area measuring 1 m 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 near- est 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.