Effect of grazing by a herbivorous gastropod Homalopoma amussitatum, a competitor for food with post-larval abalone, on a community of benthic diatoms.

ABSTRACT The effect of grazing by a small herbivorous gastropod Homalopoma amussitatum on the density and species composition of benthic diatoms was examined in the laboratory. H. amussitatum is a dominant species on exposed crustose coralline algae (CCA) along the Sanriku coast in northeastern Japan, and it has been suggested that it competes for food with postlarval abalone. The minimum densities of the gastropod required to inhibit the growth of diatoms were estimated to be <10 g/[m.sup.2] at 20[degrees]C, between 10-20 g/[m.sup.2] at 15[degrees]C, and >20 g/[m.sup.2] at 7[degrees]C. In the absence of grazing pressure, Nitzschia sp. and Psamodictyon panduriformis, which have a growth form classified as Type A (gliding prostrate type), initially formed flat communities. Amphora sp., Cocconeis sublittoralis (Type B: adhesive prostrate type) and Tabularia investiens (Type C: nonmotile upright type) subsequently increased in number. The two species of Type A were significantly affected by grazing pressure and did not increase even at a gastropod density of 10 g/[m.sup.2] at 15[degrees]C and 20[degrees]C. Types B and C diatoms were more tolerant of grazing by the gastropod than Type A species. However, the volumetric rate of ingestion of Cocconeis scutellum (Type B) by the gastropod was almost the same as for Navicula britannica (Type A) at the three experimental temperatures, when they were supplied to the gastropod independently. The digestion efficiencies of C. scutellum and N. britannica were 94.7% and 2.2%, respectively. The dietary value of C. scutellum for the gastropod H. amussitatum is thus considerably higher than that of N. britannica. In the natural CCA habitat, competitive grazing by H. amussitatum on the diatom Cocconeis spp., which is known as a major food for postlarval abalone, could significantly affect the survival and growth rates of postlarval abalone.

KEY WORDS: benthic diatom, grazing, gastropod, post-larval abalone, competition

INTRODUCTION

Benthic diatoms are the principle food for postlarval abalone (e.g., Kawamura 1996, Kawamura et al. 1998c). The abundance and species composition of benthic diatom communities on crustose coralline algae (CCA), where abalone larvae predominantly recruit (e.g., Saito 1981, Morse & Morse 1984), are suggested to significantly affect the survival and growth of metamorphosed abalone (Kawamura et al. 1998c, Takami et al. 1997, Takami et al. 2000). However, there is little information on the diatom communities on CCA surfaces in natural habitats. On CCA, there are many herbivores other than abalone (e.g., Asano et al. 1990, Kawamura et al. 1992), and their grazing controls the benthic diatom communities colonizing CCA (Kawamura 1994a, Kawamura 1994b). Herbivorous gastropods were determined to be the main grazers on benthic diatoms, controlling their abundance and species composition on CCA at several sites along the Sanriku coast, in northeastern Japan (Kawamura et al. 1992, Kawamura 1994b, Takami 2002). When the densities of gastropods were high, diatom densities were low and grazer-tolerant species dominated regardless of other environmental factors (Kawamura et al. 1992, Kawamura 1994b). Three-dimensional communities developed only when the densities of gastropods were low (Kawamura et al. 1992, Kawamura 1994b). The effect of grazing by herbivorous gastropods on microalgal composition has been studied qualitatively (e.g., Nicotri 1977, Suzuki et al. 1987, Steinman et al. 1989) but not quantitatively.

A small herbivorous gastropod Homalopoma amussitatum Gould 1861 is a dominant species on CCA along the Sanriku coast in northeastern Japan (Kawamura et al. 1992, Kawamura 1994b, Takami 2002) and has been suggested that it competes for food with postlarvae of the abalone Haliotis discus hannai Ino 1953 (Takami et al. 2001). Postlarval H. discus hannai reared with H. amussitatum showed significantly slower growth than postlarvae reared with 1-y-old H. discus hannai (Takami et al. 2001). There was no significant difference in the overall density of benthic diatoms between aquaria with H. amussitatum and with 1-y-old H. discus hannai, but the composition of diatom species differed among aquaria. The diatoms with a high dietary value for postlarval abalone, such as Cocconeis spp. (Kawamura et al. 1998c), had higher densities in aquaria with 1-y-old abalone than in aquaria with H. amussitatum (Takami et al. 2001).

In this study, the effect of grazing by H. amussitatum on the density, species composition and community structure of benthic diatoms was examined quantitatively in the laboratory. Benthic diatom communities are composed of species with various growth forms (Kawamura & Hirano 1992). Growth form influences tolerance of grazing (Kawamura & Hirano 1992, Kawamura 1994a, Kawamura 1994b) and affects ingestibility and digestion efficiency of diatoms for grazers, thus determining their nutritional value (Kawamura et al. 1995, 1998b, Roberts et al. 1999). Diatom species have been divided into 8 types (Types A to H) of growth form (see Materials and Methods). Feeding rates of the gastropod on 2 monoculture diatom strains with different growth forms (Navicula britannica Hustedt et Aleem 1951: Type A, Cocconeis scutellum Ehrenberg 1838: Type B) were measured. Diatoms with a Type A growth form are generally readily grazed, whereas those with Type B are less affected by grazing (Kawamura & Hirano 1992, Kawamura 1994a, Kawamura 1994b). However, Type A diatoms, which have low attachment strength, were easily ingested by postlarval abalone H. discus hannai (Kawamura et al. 1995) and H. iris Gmelin 1791 (Kawamura et al. 1998b) without cell rupture. The majority of ingested cells passed through the gut alive and unharmed, resulting in low digestion efficiencies and thus low abalone growth rates (Kawamura et al. 1995, Kawamura et al. 1998b). The digestibility of diatom cells has only been examined for abalone. The digestion efficiency of two diatom strains for H. amussitatum was examined. We discuss the results of the present study in light of the competition for food between postlarval abalone and H. amussitatum previously reported by Takami et al. (2001).

MATERIALS AND METHODS

Effect of Grazing on Benthic Diatom Communities

Diatom communities colonizing glass slides were held in aquaria (17 x 19 x 17.5 [cm.sup.3]) under natural light conditions at Tohoku National Fisheries Research Institute, in Shiogama, Miyagi, Japan. Aquaria were supplied with sand-filtered and temperature-controlled seawater (1.1-1.2 L/min.) at 7[degrees]C, 15[degrees]C, and 20[degrees]C. Glass slides were set on the bottom of each aquarium. Adult H. amussitatum were kept at 4 biomasses (0, 10, 20, 40 g/[m.sup.2]). The gastropods were collected in the coastal waters off Eno-shima Island and were acclimated to the experimental seawater temperatures in advance. The shell height and wet weight of gastropods ranged between 5.0-11.0 mm (7.5 [+ or -] 0.1 mm; mean [+ or -] standard error) and 0.1-0.6 g (0.22 [+ or -] 0.03 g), respectively. Two glass slides from duplicate aquaria were collected at 7-10-day intervals over 45 days. Density, species, composition, and growth form of diatoms colonizing the upper surface of the glass slides were examined under a light microscope. Diatom species were identified by a scanning electron microscope after acid cleaning (Takano & Nagumo 1987).

Growth forms of benthic diatoms are classified into 8 types (Types A to H) based on their mode of attachment, whether solitary or colonial forms, and by their motility and adhesive strengths (Kawamura & Hirano 1992, modified by Kawamura 1994a). The major diatom species colonizing glass slides in the present experiment were divided into the 4 types of growth form (Types A, B, C, and E). Type A (gliding prostrate type): solitary cells with a prostrate form, swift gliding movements, and very low adhesive strength. Type B (adhesive prostrate type): solitary cells with a prostrate form, slow movement, and high adhesive strength. Type C (nonmotile upright type): nonmotile solitary cells or simple, fan-shaped colonies standing upright with a relatively weak adhesion to the substratum. Type E (mucous thread solitary type): solitary cells or short, belt-shaped colonies attached strongly to the substratum with a mucous thread.

The differences in diatom density among experimental treatments were tested using Tukey-Kramer multiple comparison test.

Feeding Rates on Two Diatom Species

Feeding rates of H. amussitatum were measured individually at 7[degrees]C, 15[degrees]C, 20[degrees]C on 2 monoculture diatom strains (Navicula britannica: Type A, Cocconeis scutellum: Type B) by counting the diatom cell number in the feces. Cell volume of the diatoms, N. britannica and C. scutellum were 2343.4 [micro][m.sup.3] (55.4 x 9.0 x 4.7 [micro]m) and 730.8 [micro][m.sup.3] (22.0 x 15.1 x 2.2 [micro]m), respectively. Gastropods (6.4 [+ or -] 0.2 mm in shell height, 0.16 [+ or -] 0.01 g in wet weight) were reared individually, in triplicate at each temperature, in deep petri dishes (9 cm in diameter, 2 cm in depth) with diatoms growing on the bottom. All fecal pellets released by the gastropods were collected at 12- or 24-h intervals. Diatom cell numbers in the feces were calculated from the number of valves counted with a light microscope alter acid cleaning (Takano & Nagumo 1987). Gut passage time of diatoms was measured by changing diatom species, and measuring the time before new diatoms appeared in the feces.

Recently released fecal material of H. amussitatum (n = 3 for each diatom strain) reared at 20[degrees]C was observed with an inverted microscope, and the proportions of intact versus ruptured diatom cells in feces were counted. A parallel count was made of live versus ruptured cells in the diatom culture from which the fecal material was grazed. Digestion efficiency (%) was calculated as: (1-L/[L.sub.0]) x 100, where [L.sub.0] is the proportion of live cells in the source culture, and L is the proportion of live cells in the fecal pellet.

RESULTS

Effects of Grazing on Benthic Diatom Communities

At 20[degrees]C, Nitzschia sp. (Type A) initially formed flat communities in the absence of grazing by the gastropod and significantly increased at Day 15 (Fig. 1, P < 0.05). After Day 25 Amphora sp. (Type B) significantly increased (P < 0.05) and dominated. After Day 35 Tabularia investiens (Wm. Smith) Williams and Round 1986 (Type C) had significantly increased (P < 0.05) in number and was the second-most dominant species. Achnanthes brevipes var. intermedia (Kutzing) Cleve 1895 (Type E) also slightly increased in number by Day 35 but was not abundant. Nitzschia sp. and Amphora sp. almost disappeared in aquaria with gastropods (10-40 g/[m.sup.2]) at 20[degrees]C. Cocconeis sublittoralis Hendey 1951 (Type B) also decreased in number under grazing pressure. The density of Cocconeis scutellum was higher in aquaria with gastropods (10-40 g/[m.sup.2]) than without gastropods (0 g/[m.sup.2]). At Day 45 C. scutellum was dominant in aquaria with gastropods at 20 and 40 g/[m.sup.2] (P < 0.05). Remarkably, the density of T. investiens increased alter Day 35 in aquaria with gastropods at 10 g/[m.sup.2] (P < 0.05) to be comparable in aquaria without gastropods. This diatom decreased in number in aquaria with gastropods at 20 and 40 g/[m.sup.2] (P < 0.05), but was second-most dominant after C. scutellum at Day 45 (P < 0.05) (Fig. 1).

[FIGURE 1 OMITTED]

At 15[degrees]C, successions of diatom communities in aquaria without grazing (0 g/[m.sup.2]) were similar to those at 20[degrees]C, although growth rates of diatoms were lower (Fig. 2). Nitzschia sp. was most affected by grazing, and did not increase in aquaria with gastropods at 20 and 40 g/[m.sup.2] (P < 0.05). The density of Amphora sp. was significantly lower in aquaria with gastropods than without (P < 0.05), but relatively high in aquaria with gastropods at 10 g/[m.sup.2] after Day 35 (P < 0.05). Psammodictyon panduriforme (Gregory) Mann 1990 (Type A) and C. sublittoralis were generally less abundant in aquaria with gastropods, but their density in aquaria with 10 g/[m.sup.2] of gastropods was significantly higher than those in aquaria without gastropods alter Day 35 (P < 0.05). T. investiens increased to a high density in aquaria with gastropods at 10 g/[m.sup.2] after Day 35 (P < 0.05), whereas it was not abundant in aquaria without gastropods (Fig. 2) (P < 0.05).

[FIGURE 2 OMITTED]

Densities of the 3 dominant species (Nitzschia sp., Amphora sp., and C. sublittoralis) at 7[degrees]C were all lower in aquaria with gastropods than those in aquaria without gastropods (Fig. 3). However, the densities of diatoms were less affected by grazing at 7[degrees]C than at higher temperatures, and the diatoms gradually increased in number in aquaria with gastropods at 10 and 20 g/[m.sup.2] (P < 0.05). In aquaria with gastropods at 40 g/[m.sup.2], only the density of C. sublittoralis increased slightly (Fig. 3), but there was no significant difference in the density of C. sublittoralis during the experimental period (P > 0.05).

[FIGURE 3 OMITTED]

Feeding Rates on Two Diatom Species

Gut passage time of diatoms was longer at lower temperatures but within 24 h even at 7[degrees]C. Because the gastropods were feeding and producing fecal material almost continuously, the number of diatom cells in feces excreted in 24 h was considered to be equal to the amount of material ingested daily by an individual gastropod. The amount of fecal material gradually increased during the first 3 days and was almost constant after Day 3. The ingestion rate for the three seawater temperatures, calculated from the number of diatom cells excreted between Day 3 and Day 5, is shown in Table 1. The volume of each diatom strain ingested per g gastropod per day was almost the same, although the daily number of N. britannica cells ingested was less than C. scutellum. The digestion efficiency of C. scutellum at 20[degrees]C was 94.7%, whereas that of N. britannica was 2.2% (Table 1).

DISCUSSION

The succession of diatom communities, from Type A species (Nitzschia sp. and P. panduriforme) to Type B (Amphora sp. and C. sublittoralis) and Type C (T. investiens), dramatically changed with grazing by H. amussitatum. Nitzschia sp. and P. panduriforme of Type A growth form were affected more by grazing than diatoms of Types B and C (Figs. 1-3). It has been reported that Type A species are susceptible to being ingested by gastropods such as abalone (Ioriya & Suzuki 1987, Suzuki et al. 1987) and amphipods (Kawamura & Hirano 1992). The results of the present experiment showed that the two species of Type A growth form were most easily grazed by H. amussitatum.

At 15[degrees]C, the density of T. investiens in aquaria with gastropods at 10 g/[m.sup.2] was significantly higher than those in aquaria without gastropods after Day 35 (Fig. 2). At 20[degrees]C, the density of T. investiens in aquaria with gastropods at 10 g/[m.sup.2] also increased to be comparable in aquaria without gastropods (Fig. 1). The growth form of this species is easily grazed, and appeared to be abundant when grazing pressure was low in Tomarihama Bay in Miyagi (Kawamura et al. 1992). On the contrary, the density of this species was high under relatively high grazing pressure in Yoshihama Bay in Iwate (Kawamura 1994b). The dominant gastropod species were Omphalius rusticus Gmelin 1791 in Tomarihama Bay and H. amussitatum in Yoshihama Bay. Probably because H. amussitatum does not prefer to graze T. investiens (for unknown reasons other than growth form), this diatom appeared to increase when other diatoms were reduced by grazing. However, densities of this diatom were low in aquaria with gastropods at 20 and 40 g/[m.sup.2] (Figs. 1 and 2). It is suggested that H. amussitatum grazes T. investiens when food sources are limited.

Because the relative abundance of diatom species with a Type B growth form was high when the density of gastropods was high in Tomarihama Bay (Kawamura et al. 1992) and Yoshihama Bay (Kawamura 1994b), this type of diatom seemed to be relatively tolerant to grazing. The results of the present experiment showed that densities of Amphora sp. and C. sublittoralis (Type B) markedly decreased under the influence of grazing by H. amussitatum. On the other hand, C. scutellum of Type B appeared in relatively high density when grazed at 20[degrees]C (Fig. 1). A similar phenomenon was observed on settlement plates of abalone larvae in hatcheries (Ioriya & Suzuki 1987, Suzuki et al. 1987). This species may be able to increase growth under relatively high grazing pressure and/or when other diatoms are reduced by grazing, like T. investiens. However, the daily volume of C. scutellum cells ingested by the gastropod was almost the same as that of N. britannica cells when each diatom strain was supplied independently (Table 1). The digestion efficiency of C. scutellum was high, whereas most of N. britannica cells ingested by the gastropods passed through the gut alive and unbroken (Table 1). Although growth and nutritional condition of the gastropods were not examined in this study, C. scutellum seems to be a much more efficient diet than N. britannica for the growth of H. amussitatum, as previously found for abalone (Kawamura et al. 1995, Takami et al. 1996, Roberts et al. 1999). Many gastropods, such as abalone and H. amussitatum, probably graze all the microalgae growing on substrata regardless of their dietary value, with exceptions like T. investiens. Diatoms with Type B growth form are relatively hard to graze because they require considerable force to be removed, but if dislodged their cells are usually broken and release cell contents (Kawamura et al. 1995, Kawamura et al. 1998b, Roberts et al. 1999). For gastropods that can detach Type B diatom cells from substrata, these diatoms are efficient food sources because the diatom cell contents can be utilized.

Post-larval abalone can initially grow on biofilm materials including extracellular substances of diatoms, but larger postlarvae (>0.6-0.8 mm SL) need to use diatom cell contents for adequate growth (Kawamura et al. 1998c, Roberts et al. 1999). By approximately 0.8 mm SL postlarval H. discus hannai can detach Cocconeis cells efficiently, probably due to morphologic changes in the radula (Kawamura et al. 2001). Grazer-resistant algae such as Type B diatoms tend to dominate on CCA surfaces due to the high grazing intensity by gastropods. Dense patches of Cocconeis spp. were observed on CCA where postlarval and juvenile abalone were present (Takami 2002). Postlarval abalone that settled on CCA seemed to feed and grow mainly on Cocconeis. However, juvenile abalone of larger than 5-10 mm SL do not graze Cocconeis species if more favorable foods are available (Kawamura et al. 1998c), probably because the energetic value of Cocconeis ingestion becomes insufficient to support rapid growth due to their low-volume cells, prostrate growth form (Takami et al. 1996), and single layered colonies (Kawamura et al. 1998a). H. discus hannai larger than 1.8 mm SL use juveniles of the macroalga Laminoria japonica Areschoug 1851 efficiently (Takami et al. 2003). Juvenile and adult abalone graze 3-dimensional colonies of diatoms and loosely attached diatom cells simultaneously with their favored juvenile macroalgae, leaving behind prostrate diatoms with high attachment strength. Therefore Cocconeis spp. are often dominant on abalone larval settlement plates, which are pregrazed by conspecific juvenile abalone in hatcheries (Ioriya & Suzuki 1987, Suzuki et al. 1987, Seki 1997). It is considered that juvenile and adult abalone do not compete for food with postlarval abalone. On the other hand, the results of this study show that adult H. amussitatum is potentially a strong competitor for Cocconeis with postlarval abalone on CCA, as also suggested by Takami et al. (2001).

From the results of this study, the minimum densities of the gastropod H. amussitatum required to inhibit the growth of diatoms (except T. investiens) were estimated to be below 10 g/[m.sup.2] at 20[degrees]C, between 10 and 20 g/[m.sup.2] at 15[degrees]C, and above 20 g/[m.sup.2] at 7[degrees]C. On rocks covered by CCA in Tomarihama Bay, the density of herbivorous gastropods dominated by H. amussitatum was between 9.0 and 28.6 g/[m.sup.2] in 1989, and over 20 g/[m.sup.2] during the spawning season of the abalone H. discus hannai between August and October (Kawamura et al. 1992). Because the seawater temperature was over 15[degrees]C, most benthic diatoms that colonized CCA surfaces were probably eaten by gastropods. Postlarval abalone that settled on the CCA surfaces were unlikely to get sufficient food. During the study period in Tomarihama Bay, we did not collect any juvenile wild abalone from CCA rocks, although adult abalone and released juveniles lived nearby.

Sasaki and Shepherd (2001) reported that significant numbers of postlarval H. discus hannai of 5-7 days old, collected from boulders covered by CCA in Samenoura Bay, Miyagi in 1996 and 1997, showed an atrophied condition due to starvation. They hypothesized that the abundance of postlarvae of an herbivorous gastropod Tegla in the same habitat might cause food limitation and thus low survival of postlarval abalone. The results of the present study and Takami et al. (2001) indicated that a high density of gastropods such as H. amussitatum may affect abalone recruitment through competition for food.

TABLE 1.

The ingestion rate and digestion efficiency of two diatom strains
grazed by Homalopoma amussitatum at three temperatures.

                                          Ingestion rate

Temperature                      (Cells/g x Day, Mean [+ or -] SE)
([degrees]C)        Diet         ([micro][m.sup.3]/g x Day, Mean)

      7         C. scutellum     (1.5 [+ or -] 0.3) x [10.sup.6]
                                   1.1 x [10.sup.9]
                N. britannica    (3.0 [+ or -] 1.2) x [10.sup.5]
                                   7.0 x [10.sup.8]
     15         C. scutellum     (6.4 [+ or -] 0.9) x [10.sup.6]
                                   4.7 x [10.sup.9]
                N. britannica    (1.5 [+ or -] 0.2) x [10.sup.6]
                                   3.5 x [10.sup.9]
     20         C. scutellum     (8.3 [+ or -] 1.9) x [10.sup.6]
                                   6.1 x [10.sup.9]
                N. britannica    (2.6 [+ or -] 0.3) x [10.sup.6]
                                   6.1 x [10.sup.9]

                                 Digestion
Temperature                      Efficiency
([degrees]C)        Diet            (%)

      7         C. scutellum
                N. britannica
     15         C. scutellum
                N. britannica
     20         C. scutellum        94.7
                N. britannica        2.2

ACKNOWLEDGMENTS

The authors thank Masamitsu Asano for useful suggestions during the experiments, and Christopher B. Clarke and two anonymous reviewers for constructive comments of a draft manuscript.

LITERATURE CITED

Asano, M., S. Kikuchi & T. Kawamura. 1990. Effects of small herbivorous sea-snails on survival rates of the young Laminariales plants (in Japanese with English abstract). Bull. Tohoku Natl. Fish. Res. Inst. 52: 65-71.

Ioriya, T. & H. Suzuki. 1987. Changes of diatom community on plastic plates used for rearing of abalone Nordotis discus (in Japanese with English abstract). Suisanzoshoku 35:91-98.

Kawamura, T. 1994a. Taxonomy and ecology of marine benthic diatoms (in Japanese). Marine Fouling 10:7-25.

Kawamura, T. 1994b. Studies on the variation mechanisms of marine benthic diatom communities (in Japanese). Doctoral thesis, Tokyo: The University of Tokyo. 221 pp.

Kawamura, T. 1996. The role of benthic diatoms in the early life stages of the Japanese abalone (Haliotis discus hannai). In: Y. Watanabe, Y. Yamashita & Y. Oozeki, editors. Survival strategies in early life stages of marine resources. Rotterdam: A. A. Balkema. pp. 355-367.

Kawamura, T. & R. Hirano. 1992. Seasonal changes in benthic diatom communities colonizing glass slides in Aburatsubo Bay, Japan. Diatom Res. 7:227-239.

Kawamura, T., K. Okamura & H. Takami. 1998a. Growth of a benthic diatom Cocconeis scutellum var. parva, a suitable food for post-larval abalone (in Japanese with English abstract). Suisanzoshoku 46:509-516.

Kawamura, T., R. D. Roberts & C. M. Nicholson. 1998b. Factors affecting the food value of diatom strains for post-larval abalone Haliotis iris. Aquaculture 160:81-88.

Kawamura, T., R. D. Roberts & H. Takami. 1998c. A review of the feeding and growth of post-larval abalone. J. Shellfish. Res. 17:615-625.

Kawamura, T., T. Saido, H. Takami & Y. Yamashita. 1995. Dietary value of benthic diatoms for the growth of post-larval abalone Haliotis discus hannai. J. Exp. Mar. Biol. Ecol. 194:189-199.

Kawamura, T., H. Takami, R. D. Roberts & Y. Yamashita. 2001. Radula development in abalone Haliotis discus hannai from larva to adult in relation to feeding transitions. Fisheries Sci. 67:596-605.

Kawamura, T., H. Yamada, M. Asano & K. Taniguchi. 1992. Benthic diatom colonizations on plastic plates in the sublittoral zone off Oshika Peninsula, Japan (in Japanese with English abstract). Bull. Tohoku Natl. Fish. Res. Inst. 54:97-102.

Morse, A. N. C. & D. E. Morse. 1984. Recruitment and metamorphosis of Haliotis larvae induced by molecules uniquely available at the surface of crustose red algae. J. Exp. Mar. Biol. Ecol. 75:191-215.

Nicotri, M. E. 1977. Grazing effects of four marine intertidal herbivores on the microflora. Ecology 58:1020-1032.

Roberts, R. D., T. Kawamura & C. M. Nicholson. 1999. Growth and survival of post-larval abalone (Haliotis iris) in relation to their development and diatom diet. J. Shellfish Res. 18:243-250.

Saito, K. 1981. The appearance and growth of 0-year-old Ezo abalone. Bull. Jap. Soc. Sci. Fish 47:1393-1400.

Sasaki, R. & S. A. Shepherd. 2001. Ecology and post-settlement survival of the ezo abalone, Haliotis discus hannai, on Miyagi coasts, Japan. J. Shellfish Res. 20:619-626.

Seki, T. 1997. Biological studies on the seed production of the northern Japanese abalone, Haliotis discus hannai Ino (in Japanese with English abstract). Bull. Tohoku Natl. Fish. Res. Inst. 59:1-71.

Steinman, A. D., C. D. McIntire, S. V. Gregory & G. A. Lamberti. 1989. Effects of irradiance and grazing on lotic algal assemblages. J. Phycol. 25:478-485.

Suzuki, H., T. Ioriya, T. Seki & Y. Aruga. 1987. Changes of algal community on the plastic plates used for rearing the abalone Haliotis discus hannai. Nippon Suisan Gakkaishi 53:2163-2167.

Takami, H. 2002. Studies on the feeding, growth and survival in early life stages of an abalone Haliotis discus hannai (in Japanese). Doctoral thesis, Tokyo: The University of Tokyo. 220 pp.

Takami, H., T. Kawamura & Y. Yamashita. 1996. Dietary value of benthic diatoms for the growth of juvenile abalone Haliotis discus hannai (in Japanese with English abstract). Suisanzoshoku 44:211-216.

Takami, H., T. Kawamura & Y. Yamashita. 1997. Contribution of diatoms as food sources for post-larval abalone Haliotis discus hannai on a crustose coralline alga. Moll. Res. 18:143-151.

Takami, H., T. Kawamura & Y. Yamashita. 2000. Starvation tolerance of newly metamorphosed abalone Haliotis discus hannai. Fisheries Sci. 66:1180-1182.

Takami, H., D. Muraoka, T. Kawamura & Y. Yamashita. 2003. When does abalone Haliotis discus hannai begin to utilize brown macroalgae? J. Shellfish. Res. 22:795-800.

Takami, H., T. Kawamura, H. Ito, M. Seito, S. Yanagiya & Y. Yamashita. 2001. Competition for food between post-larval abalone and two species of herbivorous gastropods (in Japanese with English abstract). Bull. Tohoku Natl. Fish. Res. Inst. 64:43-51.

Takano, H. & T. Nagumo. 1987. Methods to study red tide organisms. Chap. 5 Diatoms (in Japanese). In: A guide for studies of red tide organisms. Tokyo: Japan Fisheries Resource Conservation Association. pp. 102-120.

TOMOHIKO KAWAMURA, (1), * HIDEKI TAKAMI, (2) AND YOH YAMASHITA (3)

(1) Ocean Research Institute, The University of Tokyo, Nakano, Tokyo 164-8639, Japan; (2) Tohoku National Fisheries Research Institute, Shiogama, Miyagi 985-0001, Japan; (3) Maizuru Fisheries Research Station, Field Science and Education Research Center, Kyoto University Maizuru, Kyoto 625-0086, Japan

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