Distribution of the sea urchin Hemicentrotus pulcherrimus along a shallow bathymetric gradient in Onagawa Bay in Northern Honshu, Japan.

ABSTRACT Distribution of the sea urchin Hemicentrotus pulcherrimus was monitored monthly or bimonthly from April 1998 to May 1999 at a 100 [m.sup.2] permanent site in intertidal to subtidal zones at depths of up to 2.8 m in Onagawa Bay, northern Honshu, Japan. Factors causing seasonal demographic changes were analyzed from vertical algal vegetation, sea urchin size, gonad development, and gut content. The highest density of H. pulcherrimus was found on algal turf on boulders at the depth of 0-0.3 m. Migration of adult sea urchins on crustose corallines at the depth of 0.3-2.8 m to the algal turf and subsequent inhabitation in more suitable boulder habitat are suggested from November to March, when Acrosorium polyneurum, which is their main food, grew dominantly. As the high gut content of crustose coralline of the sea urchins on crustose corallines resulted in significantly lower gonad indices, it is likely that migration is caused by their high foraging activity for A. polyneurum to ensure gonad development. The growth of the sea urchins on algal turf was ensured by Chondrus spp. as main food.

KEY WORDS: sea urchin, Hemicentrotus pulcherrimus, distribution, gonad development, gut content, migration, Acrosorium polyneurum.

INTRODUCTION

The sea urchin Hemicentrotus pulcherrimus (A. Agassiz 1863) is found in intertidal and subtidal zones from Kyushu to Rebun Island, Hokkaido, Japan and in Korea and China (Shigei 1995, Agatsuma 2001a). This sea urchin is an important fisheries resource in shallow waters in the coastal regions of the southern Japan Sea from Fukui Prefecture. The brands "Echizen Uni" in Fukui Prefecture and "Shimonoseki Uni" in Yamaguchi Prefecture are well known. In Fukui, stones were introduced in 1910 to enhance the sea urchin' s habitat (Andrew et al. 2002, Agatsuma et al. 2003). Adult sea urchins with poor gonad development have been transplanted to kelp forests, where gonad development improves (Andrew et al. 2002, Agatsuma et al. 2003). In addition, seed production was initiated in a Yamaguchi hatchery in the 1960s (Sakai et al. 2003). The seeds (juveniles) of H. pulcherrimus were released in Saga, Shimane and Fukui Prefectures, and the number exceeded 1000,000 individuals in 1993, releases ranged from 390,000-890,000 individuals until 2000 (Agatsuma et al., 2003).

Quantifying seasonal patterns in density and size distributions among different habitats is necessary for managing and sustaining populations of sea urchins. In addition, the seasonal habitat selection relative to age and associated with algal assemblage as food resources that ensure growth and gonad development should also be clarified. In shallow waters in the Sea of Japan, Hokkaido, 0-y-old Strongylocentrotus nudus inhabit crustose coralline communities where the larvae settle (Taniguchi et al. 1994, Sano et al. 1998) throughout the year. Sea urchins that are >1 y old migrate to the kelp Laminaria religiosa bed in an intertidal zone, where their gonads are ensured to develop for reproduction from summer to autumn. They then return to the crustose corallines to avoid the strong wave action in winter (Agatsuma 2001b). A similar seasonal migration of S. nudus is also found in Pacific coastal waters, where an Eisenia bicyclis forest grows in subtidal shallow waters (Sano et al. 1998, Sano et al. 2001). Adult Paracentrotus lividus migrate from a pebble area where larvae settle to a Cymodocea nodosa sea grass bed in relation to a change in food habit (Fernandez et al. 2001). The migration of Sphaerechinus granularis from Phymatolithon communities to Zostera marina or macroalgal beds is also related to changes in food habit (Guillou & Michel 1993). Loxechinus albus with >45 mm diameter also migrate from the intertidal zone where larvae settle to brown macroalgal beds at a depth of 4-15 m (Contreras & Castilla 1987). However, except for S. nudus, the principal purpose for migration is not clear. And that, there is no known reason for sea urchins to migrate, and the foods that they forage have not been identified by analysis of their gut content. In the life history of H. pulcherrimus, seasonal changes in the vertical distributions and the algal foods in relation to algal vegetation are also unknown.

In the present study, we monitored the density and test diameter of a H. pulcherrimus population in relation to the depth, bottom characteristics, and vertical algal vegetation from intertidal and subtidal zones in the Pacific near shore waters of northeastern Honshu. An analysis of the gut content was undertaken to determine the foods for gonad development and growth. Consequently, the factors contributing to seasonal demographic changes were suggested.

MATERIALS AND METHODS

Site Characteristics

A monthly or bimonthly survey was conducted in the intertidal and subtidal zones at Sashigahama (38[degrees]28'N, 141[degrees]29'E) in Onagawa Bay, Miyagi, from April 1998 to May 1999 (Fig. 1). Previously, a study site was determined from predominance of H. pulcherrimus by SCUBA diving observation. A survey was performed using one fixed transect (50 m long x 2 m wide) as the study site placed perpendicularly to the coast line.

[FIGURE 1 OMITTED]

In April 1998, the bottom profile at the study site was sketched precisely using a 1 x 1 m quadrat by SCUBA. Depth was measured with a water-pressure gauge (Japan Aqualung Co., Ltd.) at an interval of 1 m along the leaded rope placed at the center of the study site, and compensated at the level of the shallowest water. Algal vegetation at the study site in each quadrat was observed using SCUBA and video-recorded (Handycam, DCR-TRV7, Sony Corporation). Unidentified algae in the field were collected and identified in the laboratory.

The mean surface water temperature every ten days during the present study and the averages for 30 y from 1968-1997 were referred to the data at Enoshima (38[degrees]24'N, 141[degrees]36'E) near the study site, measured by Miyagi Prefecture Fisheries Research and Development Center.

Density and Size Analysis

In the study site, a 1 x 1 m quadrat was used, and the test diameter of H. pulcherrimus was measured in each quadrat with a vernier caliper (1 mm accuracy); the results were recorded on aqua-notes by SCUBA. The sea urchins were replaced in the same quadrates. No survey was performed at a distance of 0-25 m in January 1999 because of the high wave action.

Strongylocentrotus nudus and S. intermedius also distributed in the study site and their density in each quadrat was also recorded. Throughout the year, S. nudus was found on deep crustose corallines with density of 4.5-8.4 individuls/[m.sup.2]. Low density of <2.5 individuls/[m.sup.2] was found for S. intermedius.

Gonad Analysis

To determine the gonad development and feeding habits during the study, except for April 1998, a 50 m leaded rope was set up at a distance of 15 m west of the site, where similar algal vegetation was observed. Twenty specimens of H. pulcherrimus larger than 3 cm in diameter, which exceeds the mature size (Kawana 1938), were collected from algal turf along the line. Similarly, 5-10 specimens were collected at crustose corallines. The test diameter and body weight (g wet weight) were measured using a vernier caliper (0.1 mm accuracy) and an electronic balance (0.01 g accuracy). Gonad wet weight was also measured (0.01g accuracy), and gonad index (gonad weight x 100/body weight) was calculated. Part of the gonad was preserved in 20% formalin for 24 h, and after that, in 10% formalin. Using standard histological techniques, serial cross sections (6 [micro]m) were cut through the center of a gonad and stained with Mayer's hematoxylin and eosin. Histological sections were classified according to Fuji (1960): Stage I, recovering; Stage II, growing; Stage III, premature; Stage IV, mature; and Stage V, spent.

Gut Content Analysis

Five specimens with a test diameter in excess of 3 cm were used to analyze the gut content on algal turf and crustose corallines. The gut content for each individual was obtained and filtered on a nylon net with a mesh size of 350 [micro]m. The component of fractions <350 [micro]m was excluded because it was difficult to sort. First, the components were divided into three groups, algae, animals and minerals, according to shape, color, and hardness with the use of a stereomicroscope. Furthermore, algae were classified into a family, genus, or species from its specific cell structure using a dissecting microscope. After that, each food item sorted was sucked on filter paper (Whatman GF/C) and dried for 12 h at 80[degrees]C in a hot-air convection oven and then weighed using a microbalance (1 mg accuracy).

Statistical Analysis

Statistical difference in densities of H. pulcherrimus at each four of the characterized areas in the study site among months and the densities among four areas was analyzed by two-way repeated ANOVA and Scheff'e's multiple comparison test. Significant difference in the gonad indices on algal turf and crustose corallines among months was analyzed by one-way factorial ANOVA and Scheffe's multiple comparison test. The difference in indices between the two vegetation types were analyzed by unpaired t-test after confirming no significant difference in variance between them by F-test. All the data showed normal distribution and homogeneous variance by Shapio-Wilk's W-test and Cochran's test, respectively.

RESULTS

Site Characteristics and Seawater Temperature

At the study site, boulders formed >50% of the substrata at the study site at distances of 10-17, 25-34, and 42-50 m. In the other areas, undulating rocks with ditches and holes in addition to boulders were present (Fig. 2).

[FIGURE 2 OMITTED]

The depth and seasonal changes in the vegetation of the dominant algae with these coverage of ca. >50% in the study site are shown in Figure 3. The area at a distance of 0-10 m is in the intertidal zone. Subsequently, the area sloped gently from 10-24 m at depths of up to 0.3 m and steeply from 24-50 m at depths of 0.3-2.8 m. From the upper to the lower intertidal zone, Gloiopeltis furcata, Analipus japonicus, and Sargassum fusiformis grew all year round. Sargassum thunbergii generally grew below S. fusi-formis, except for the period from September to December, when Chondria crassicaulis grew dominantly. From the lower intertidal zone to the subtidal gentle slope at depths of up to 0.3 m, Chondrus ocellatus and C. verrucosus grew dominantly from April to December. However, their growth zone was reduced to the lower intertidal zone in March and May the following year. From September to December, Grateloupia livida and Acrosorium polyneurum colonized the Chondrus growth zone. In March and May, A. polyneurum grew dominantly at a depth of 0-0.2 m. Sargassum yezoense and S. micracanthum grew on rocks at a depth of 0.3 m all year round. Those sargasso algae grew abundantly in June and July. After dieback, the holdfasts and stipes remained from September to March. At the deeper zone of >0.3 m, crustose corallines dominated, whereas Dilophus okamurae grew at a depth of 2.1-2.8 m from September to March and dominantly from October to January. The study site was characterized by depth, algal vegetation, and bottom character; the intertidal zone, the algal turf with gentle slope at the depth of 0-0.3 m, the upper steep-sloped crustose corallines at the depth of 0.3-1.0 m, and the lower steep-sloped crustose corallines at the depth of 1.0-2.8 m.

[FIGURE 3 OMITTED]

Except for the period from February to April and August, the water temperature during this study was markedly higher than the average. In particular, the deviation showed high values of 3.8[degrees]C in late December 1998 and 2.0-2.4[degrees]C in January and late April 1999 (Fig. 4).

[FIGURE 4 OMITTED]

Vertical Distribution

Seasonal changes in the density of H. pulcherrimus on the 4 characterized areas in the study are shown in Figure 5. Significant difference in the density among 4 areas (df = 3, MS = 3951.505, F = 163.587, P < 0.0001) and month (df = 9, MS = 9.898, F = 4.529, P < 0.0001) was found. Significant correlation between the area and month was also found (df = 27, MS = 75.719, F = 6.872, P < 0.0001). The densities on algal turf were significantly higher than those on the other areas throughout the year (P < 0.01). There, the sea urchins were found beneath the boulders. Subsequently, their densities on upper crustose corallines were significantly higher than those on intertidal and lower crustose corallines, with the exception of September 1998 and March and May 1999 (P < 0.01).

[FIGURE 5 OMITTED]

The densities on the intertidal zone were low all year round. On algal tuff, the densities from April to December 1998 ranged from 14.4-17.9 individuals/[m.sup.2], and no significant difference was found (P > 0.05). Then, the density significantly rose to 28.3 individuals/ [m.sup.2] in March (P < 0.05). In May, it was also higher than from April to November the previous year (P < 0.05).

On the upper crustose corallines, the densities from November 1998 to January 1999 were significantly higher than those from May to September 1998 (P < 0.05). In addition, those in December and January were higher than that in October (P < 0.01). In particular, in January, the density reached a peak of 11.6 individuals/ [m.sup.2]. Whereas, it significantly fell in March and May 1999, when it reached a peak on algal tuff (P < 0.01).

On the lower crustose corallines, the densities were low all year round. In January, the density reached a peak of 3.3 individuals/ [m.sup.2], significantly higher than that each month the previous year, with the exception of November (P < 0.01). The density in November was higher than those in May, June, and September 1998 (P < 0.05). The density in March and May 1999 was significantly lower than that in January (P < 0.01), as observed on the upper crustose corallines. Thus a marked increase in the density of urchins on the algal turf from November to March was found.

The density on the algal tuff in March 1999 was significantly higher than that in April 1998 (P < 0.01), whereas that on the upper crustose corallines showed a significantly low value (P < 0.05).

Size Frequency Distribution

Changes in the test diameter frequency distribution of H. pulcherrimus in each of the 4 areas are shown in Figure 6. At each area, sea urchins of 30-39 mm test diameter were predominant. On algal tuff, the mode of test diameter distribution clearly shifted from 36-38 mm to 40-42 mm from June to December 1998. On the other hand, the sea urchins with 32-36 mm in test diameter increased and the mode shifted to 34-38 mm in March and May 1999, when the sea urchin densities rose significantly. On the upper crustose corallines, the mode was around 40 mm from June to October, whereas urchins of 30-38 mm test diameter increased from November to January. Moreover, sea urchins of 32-36 mm test diameter were clearly found in each area in April and May 1998.

[FIGURE 6 OMITTED]

Gonad Development Process

The gonad development of the sea urchins was classified into five stages from histological observation as shown in Figure 7, and the seasonal changes on algal turf and crustose corallines were shown in Figure 8. From June to September, the gonads of the sea urchins at each algal community were in the recovering stage, with small numbers of oocytes and spermatocytes, with nutritive phagocytes filling the lumen (Fig. 7, 1A, 1B). Then, they progressed from the growing stage (Fig. 7, 2A, 2B), with increasing numbers of oocytes or spermatocytes along the acinal wall in October, to the mature stage (Fig. 7, 4A, 4B), in which most of the lumen is filled with ova and spermatozoa, in December or January. For long periods from January to June, the spent stage continued, with some relict ova and spermatozoa and empty spaces in the lumen (Fig. 7, 5A, 5B).

[FIGURES 7-8 OMITTED]

Seasonal changes in the gonad indices of the sea urchins at each community are shown in Figure 9. At each community, a significant seasonal difference in gonad indices was found (Algal turf: df = 9, MS = 371.4, F = 35.956, P < 0.0001, Crustose coralline: df = 9, MS = 32.1, F = 3.968, P < 0.0026). There was no statistical difference in the gonad indices at algal turf from May to September 1998, when those ranging from 11.9-13.8 were in the recovering stage (P > 0.05). Then, the indices significantly rose to 18.5 in October, when gonad development was in the growing and premature stages (P < 0.01). The indices significantly fell to the minimum value of 5.4 in March 1999 (P < 0.05) and remained at that value until May. The gonad indices on crustose corallines ranged from 5.0-11.2 from May 1998 to January 1999, and no seasonal difference in the indices was found (P > 0.05). In March, the indices showed a minimum value of 2.5, similar to those found on algal turf. Except for June, December, and January, the gonad indices on algal turf were higher than those at crustose corallines (P < 0.05).

[FIGURES 9 OMITTED]

Gut Contents

The gut contents of H. pulcherrimus at each algal community are identified as shown in Table 1. In the gut contents of sea urchins on algal turf, the algae of 15 species, 7 genera and 2 unidentified taxa were found. These were small algae, except for Sargassum spp. The seagrass Zosteraceae, the attached diatom Bacillariophyceae, a terrestrial plant, and animals such as Gastropoda, Bivalvia, and Crustacea were also found. In those components, Sargassum spp., Chondrus spp., Acrosorium polyneurum, and Crustacea occurred all year round. On crustose corallines, a similar number of species, genera and taxa of algae occurred despite the fact that few algal species grow, and the other components were similar to those found on algal turf. Crustose coralline, A. polyneurum, and Crustacea occurred all year round.

The seasonal changes in the mean weight percentage of each of the 6 main algal components to total gut contents are shown in Figure 10. On algal turf, Chondrus spp., A. polyneurum, and Sargassum spp. showed high percentages, reflecting the dominant vegetation. The percentage of Chondrus spp. was high from July to October. From November to March, the percentage of A. polyneurum ranged 30% to 40%, higher than that of five other algae. In May 1999, the percentage of Sargassum spp. abruptly rose to 49%, in contrast to fall in that of A. polyneurum. On crustose corallines, a high percentage of crustose coralline was found all year round; particularly, the percentage reached 49% to 78% from October to May. In June, July and September, that percentage fell to <21%. In June, the percentage of Sargassum spp. abruptly rose to 42%, higher than that of other algae. In September, C. hubbsii also showed high percentage. The percentage of crustose coralline in May 1999 was higher than that in May 1998.

[FIGURE 10 OMITTED]

DISCUSSION

The densest habitat of H. pulcherrimus was found on algal turf at a depth of 0-0.3 m, where boulders dominated. Similarly, a dense distribution beneath boulders in shallow waters is found in other regions in Japan (reviewed by Agatsuma 2001a). However, their low density on crustose corallines at a depth of >1.0 m with boulders shows that the distribution of H. pulcherrimus is not restricted by the factor of bottom characteristics alone. The seasonal changes in density suggest that the sea urchins migrate from crustose corallines to algal turf from November to March. Juvenile H. pulcherrimus with 0.8-4.5 mm in test diameter were observed in Amphiroa dilatata and the roots of Phyllospadix japonicus in shallow waters of the Japan Sea, Fukui (Kawana 1938). However, it is unknown where the larvae settle and metamorphose. The migration from crustose corallines raises the possibility that the larvae settle on crustose corallines, as do Strongylocentrotus purpuratus and S. franciscanus (Cameron & Schroeter 1980, Rowley 1989), S. nudus (Taniguchi et al. 1994, Sano et al. 1998), and S. droebachiensis (Balch & Scheibling 2000).

The gonads of Strongylocentrotus spp. in a kelp forest grow larger than they do in barren grounds (Agatsuma 2001b, Gonor 1973, Lang & Mann 1976, Pearse 1980, Wharton 1980, Johnson & Mann 1982, Keats et al. 1984, Scheibling & Stephenson 1984, Sivertsen & Hopkins 1995, Meidel & Scheibling 1998). The difference in gonad mass is caused by food availability at each habitat (Lang & Mann 1976, Sivertsen & Hopkins 1995). Meidel and Scheibling (1998) clarified the difference between the food availability of S. droebachiensis in kelp (Laminaria longicruris) forest and barren grounds from quantitative gut content analysis.

In the present study, gut content analysis showed that the foliose algae Chondrus spp., A. polyneurum, and Sargassum spp. were main foods for H. pulcherrimus on algal tuff. The high percentage of crustose coralline in the gut contents of the sea urchins on crustose corallines results in lower gonad indices than those on algal turf. From changes in size frequency distributions, seasonal growth was clearly found from June to December. In the gut contents of the sea urchins on crustose corallines during this period, the percentage of crustose coralline was lower than that in other months, as Sargassum spp., Codium hubbsii and the other algae were supplied as drift algae from shallow waters. It is more likely that those drift algae contribute the growth of the sea urchins on crustose corallines. The down-shift in the modal size of sea urchins on the algal turf during the migration period could be attributed to the immigration of smaller, low-growing ones from crustose corallines in deeper waters. In addition, the growth of sea urchins on algal turf is considered to be mainly supported by Chondrus spp., which showed a high weight percentage in the gut contents until October.

The histological observation of gonad and the seasonal changes in gonad indices show that spawning occurs from January to May, reaching a peak from January to March, as it does in other regions in western Japan (Agatsuma 2001a). Gonad size reached a peak corresponding to maturation and spawning from October to March. The rise in the weight percentage of crustose coralline, which was more than approximately 50% in the gut contents of the sea urchins on crustose corallines after September, is related to a decrease in the supply of drift algae from shallow waters. Therefore, these findings suggest that the grazing activity switched to an active and mobile mode, as found in S. purpuratus and S. franciscanus (Mattison et al. 1977, Russo 1979, Harrold & Reed 1985) and Evechinus chloroticus (Andrew & Stocker 1986), and the movement to algal turf in shallow waters was triggered. As A. polyneurum grew dominantly from October to March and showed a high percentage in the gut contents, this alga can be considered to be food that ensures gonad development and success in the reproduction of the sea urchins that migrate from crustose corallines to algal turf. Thus, it is suggested that the migration is related to the search for the algal food A. polyneurum.

In the meanwhile, the density of H. pulcherrimus on algal turf in March 1999 was higher than that in April and May 1998. In addition, the percentage of crustose coralline in the gut contents on crustose corallines in May 1999 was significantly higher than that in May 1998. These results may suggest that much higher water temperatures during winter in 1999 than those of average years reduced the algal communities as found in Oshika Peninsula near the study site in 1980s (Taniguchi 1991), causing algae to subsequently drift, and resulted in the migration of many sea urchins with poor gonad development to shallow waters. For the sympatric sea urchin S. nudus, no 0-1-y-old juveniles with a food habit of attached diatoms and small algae migrate from crustose corallines, where larvae settle, to a kelp (L. religiosa) forest (Agatsuma 2001 b). In the present study, the pattern of migration of juvenile H. pulcherrimus is unclear, as few juveniles of test diameter less than 10 mm were observed. Maturation size is considered to be at 26 mm in test diameter in Fukui (Kawana 1938). Whereas, the difference in maturation size among localities and maturation age is unknown. The changes in test diameter distribution may suggest that over 2-y-old urchins with a test diameter of 32-36 mm were the ones that mainly migrated. Thus, it is unclear whether those migrating sea urchins correspond to the first maturation-size group.

After the migration of H. pulcherrimus, no return to crustose corallines was observed. The residence of H. pulcherrimus on algal turf is likely to be related to food supply, but it additionally ensures a suitable habitat beneath boulders, which reduce the action of the waves. In addition, a study on the morphological characteristics with thick test in relation to attachment strength of the foot tube, and tolerance of test and spine from abrasion would contribute to understanding their adaptation to a habitat in shallower waters. In the areas in Yamaguchi and Kanagawa Prefectures where H. pulcherrimus is observed, the large brown algae Sargassaceae and Laminariales grow sympatrically (Agatsuma 2001a). The interactions between specimens of H. pulcherrimus and the marine forest should be studied seasonally.

Significant gonad enhancement of H. pulcherrimus on algal turf was found from September to October. The maximum gonad index of 18.5 in October coincides with that of 17-19 at the fishing grounds in Saga, where the most rapid growth in western Japan was reported (Ito et al. 1989, Shimazaki et al. 1987), although lower than that of 25 in Oshoro Bay, Hokkaido (Agatsuma & Nakata 2004). The seasonal growth and gonad enhancement on algal turf are likely to be caused by Chondrus spp., which grew dominantly and showed a high percentage in gut contents. Therefore, the dietary effect of Chondrus spp. and A. polyneurum as the main food for migrating sea urchins on growth and gonad development should be evaluated by means of a rearing experiment.

ACKNOWLEDGMENTS

The authors thank Y. Sato, former Director-general, and the staff of Miyagi Prefecture Fisheries Research and Development Center for providing water temperature data. The authors also thank the staff of Sashigahama Fisheries Cooperative Association for their cooperation in our field study. This study was supported in part by a Grant-in-Aid for Scientific Research (No.11660177) from the Ministry of Education, Culture, Sports, Science, and Technology in Japan.

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YUKIO AGATSUMA, (1) * HIROKAZU YAMADA (2) AND KAZUYA TANIGUCHI (1)

(1) Laboratory of Marine Plant Ecology, Graduate School of Agricultural Science, Tohoku University, Aoba, Sendal, Miyagi 981-8555, Japan; (2) Shizuoka Prefectural Fisheries Experimental Station, Izu Branch, Shirahama, Shimoda 415-0012, Japan

* Corresponding author. E-mail: [e-mail]

TABLE 1.
Gut contents of Hemicentrotus pulcherrimus at algal turf (open
circles) and crustose corallines (filled circles).

                                                1998

Species                           May      Jun.      Jul.      Sep.

Ulva pertusa                    (A) (B)   (A)       (A)
Cladophora conchopheria                             (A)
Codium hubbsii                                (B)   (A) (B)   (A) (B)
Ralfsia spp.                                  (B)   (A) (B)   (A)
Dictyota dichotoma                        (A)       (A)       (A) (B)
Dilophus okamurae                         (B)       (A) (B)   (A) (B)
Elachista okamurae                                      (B)
Sargassum spp.                  (A) (B)   (A) (B)   (A)       (A) (B)
Crustose corallines             (B)       (A) (B)   (A) (B)   (A) (B)
Corallina spp.
Gelidium elegans                (A) (B)   (A) (B)   (A) (B)   (A) (B)
Chondrus spp.                   (A)       (A) (B)   (A) (B)   (A) (B)
Carpopeltis spp.                (A) (B)   (A)       (A) (B)   (A)
Hypnea spp.                                   (B)
Ahnfeltiopsis flabelliformis    (A) (B)   (A) (B)
A. paradoxa                               (A) (B)
Plocamium telfairiae                      (A) (B)   (A) (B)   (A) (B)
Lomentaria catenata             (A)       (A) (B)   (A) (B)
L. hakodatensis                           (A) (B)             (A)
Heterosiphonia pulchra          (A) (B)   (A) (B)
Acrosorium polyneurum           (A) (B)   (A) (B)   (A) (B)   (A) (B)
Laurencia spp.                                          (B)   (A) (B)
Polysiphonia spp.
Symphyocladia latiuscula                  (A) (B)
S. marchantioides                                   (A) (B)
Zosteraceae                     (A)       (A) (B)   (A) (B)   (A) (B)
Bacillariophyceae
Terrestrial plant               (A)       (A)           (B)
Hydrozoa                                  (A) (B)   (A)
Bryozoa                         (A) (B)                 (B)   (A) (B)
Gastropoda                                              (B)   (A) (B)
Eumalacostraca                  (A) (B)   (A) (B)   (A) (B)
Crustacea                       (A) (B)   (A) (B)   (A) (B)   (A) (B)
Feather of terrestrial insect
Feather of bird                           (A)                 (A)
Plastic                                   (A)
Others *                        (A) (B)   (A) (B)   (A) (B)   (A) (B)

                                           1998

Species                          Oct.      Nov.      Dec.

Ulva pertusa
Cladophora conchopheria
Codium hubbsii
Ralfsia spp.                    (A) (B)   (A) (B)   (A) (B)
Dictyota dichotoma              (A)       (A)       (A) (B)
Dilophus okamurae               (A) (B)   (A) (B)   (A) (B)
Elachista okamurae
Sargassum spp.                  (A) (B)   (A) (B)   (A) (B)
Crustose corallines             (A) (B)   (A) (B)   (A) (B)
Corallina spp.
Gelidium elegans                (A)                     (B)
Chondrus spp.                   (A) (B)   (A) (B)   (A) (B)
Carpopeltis spp.                (A)
Hypnea spp.
Ahnfeltiopsis flabelliformis
A. paradoxa                     (A)
Plocamium telfairiae                      (B)       (A) (B)
Lomentaria catenata                       (A) (B)   (A) (B)
L. hakodatensis                 (A)       (A) (B)   (A)
Heterosiphonia pulchra                    (B)
Acrosorium polyneurum           (A) (B)   (A) (B)   (A) (B)
Laurencia spp.
Polysiphonia spp.               (A)
Symphyocladia latiuscula        (A)       (A)       (A)
S. marchantioides                             (B)
Zosteraceae                     (A) (B)       (B)   (A) (B)
Bacillariophyceae                                   (A)
Terrestrial plant               (A) (B)             (A) (B)
Hydrozoa
Bryozoa                         (A) (B)
Gastropoda                                          (A)
Eumalacostraca                  (A)
Crustacea                       (A) (B)   (A) (B)   (A) (B)
Feather of terrestrial insect
Feather of bird
Plastic                                                 (B)
Others *                        (A) (B)   (A) (B)   (A) (B)

                                           1999

Species                          Jan.      Mar.       May

Ulva pertusa
Cladophora conchopheria
Codium hubbsii
Ralfsia spp.                    (A) (B)   (A) (B)   (A) (B)
Dictyota dichotoma              (A)
Dilophus okamurae               (A) (B)   (A) (B)   (A) (B)
Elachista okamurae
Sargassum spp.                  (A) (B)   (A) (B)   (A) (B)
Crustose corallines             (A) (B)   (A) (B)   (A) (B)
Corallina spp.                            (A) (B)
Gelidium elegans                    (B)   (A) (B)       (B)
Chondrus spp.                   (A) (B)   (A) (B)   (A) (B)
Carpopeltis spp.                          (A)
Hypnea spp.
Ahnfeltiopsis flabelliformis    (A)
A. paradoxa                               (A)
Plocamium telfairiae            (A) (B)   (A)
Lomentaria catenata             (A)       (A)           (B)
L. hakodatensis                     (B)   (A) (B)
Heterosiphonia pulchra
Acrosorium polyneurum           (A) (B)   (A) (B)   (A) (B)
Laurencia spp.
Polysiphonia spp.
Symphyocladia latiuscula        (A)       (A)       (A)
S. marchantioides
Zosteraceae                     (A) (B)   (A) (B)   (A) (B)
Bacillariophyceae
Terrestrial plant                   (B)   (A)           (B)
Hydrozoa
Bryozoa                         (A)
Gastropoda                      (A)       (A)
Eumalacostraca                            (A)       (A)
Crustacea                       (A) (B)   (A) (B)   (A) (B)
Feather of terrestrial insect
Feather of bird
Plastic                             (B)   (A)
Others *                        (A) (B)   (A) (B)   (A)

* Residual matters including the unclassified plants and animals,
and sand.

(A) (open circles)

(B) (filled circles).