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Fine structure, histochemistry, and morphogenesis during Excystment of the Podocysts of the giant jellyfish Nemopilema Nomurai (scyphozoa, Rhizostomeae).


The giant jellyfish Nemopilema nomurai Kishinouye 1922 is one of the biggest scyphozoan jelly fishes in the world, attaining a bell diameter of 2 m and a wet weight of 200 kg (Kishinouye, 1922; Shimomura, 1959). This jellyfish has caused massive blooms in the East Asian marginal seas (i.e., the Bohai, Yellow, East China and Japan seas) almost annually since 2002, although in the last century such mass occurrences were very rare, occurring at about 40-year intervals (Kishinouye, 1922; Shimomura, 1959; Nishimura, 1959, 1961; Yasuda, 2004; Kawahara et at, 2006; Uye, 2008). Medusae of this species are thought to be released as ephyrae from benthic polyps residing in the Yellow and East China Seas during late spring and early summer, and the growing medusae are then transported into the Sea of Japan by the Tsushima Current (Kawahara et al.7 2006; Reizen and Isobe, 2006; Yoon et aL, 2008). Frequent recent blooms are causing concern about the possible settlement of planula larvae and establishment of new populations in Japanese coastal waters (Uye, 2008; Ikeda et ai., 2011).

Like most scyphozoan species, N. nomurai has a life cycle that consists of the alternation of a sexual (planktonic) medusa phase and an asexual (benthic) polyp phase; the latter may play an important role in determining the medusal population size for the following season (Grondahl, 1988; Lo et aL, 2008). Although Aurelia aurita (Linnaeus 1758) and its sibling species (Dawson and Martin, 2001), which annually cause blooms in coastal waters worldwide, asexual ly reproduce primarily by budding, which directly increases polyp abundance (Han and Uye, 2010; Thein et al., in press), N. nomurai reproduces asexually by production of podocysts, from which new polyps excyst (Kawahara et aL, 2006). Therefore, the podocysts of TV. nomurai are a crucial stage for the population dynamics of polyps and subsequent blooms of medusae.

A podocyst is an encapsulated dormant stage produced beneath the pedal disc of the polyps of many rhizostome and semaeostome jellyfish species (Arai, 2009). The histological characters of podocysts have been examined only in semaeostome species of jellyfish, including A aurita (Chapman, 1968, 1970; Thein et at, in press), Chrysaora quinquecirrha (Desor 1848) (Blanquet, 1972; Black et al., 1976; Black, 1981), and Cyanea lamarcki Peron and Lesueur 1809 [as Cyanea palmstruchi Swartz 1809] (Widersten, 1969). Those studies reveal the fine structure of a mass of cyst cells encapsulated in a chitinous capsule, with nutrient reserves of proteins, carbohydrates, and lipids, and a change in cellular structure with age. However, the biological properties of podocysts are still unknown in rhizostome jellyfishes including N. nomurai. A question arises as to how the podocysts of N. nomurai differ from those of semaeostome species in fine structure and chemical content. The histological process during excystment is not well understood in scyphozoan jellyfishes, and this is to be clarified in N. nomurai. Furthermore, changes of internal structure associated with age are important for the estimation of potential longevity of N. nomurai podocysts.

We here examine the fine structure, chemical content, and structural changes during aging and excystment of the podocysts of N. nomurai to understand the mechanisms of their dormancy and excystment.

Materials and Methods

Production of podocysts

Podocysts of Nemopilema nomurai were produced by the polyps of our stock cultures established in 2006, 2007, and 2009 by means of the artificial fertilization described by Ohtsu et ai (2007). In brief, portions of ovaries and testes were excised from medusae caught near Oki Island, in the southern Sea of Japan, and placed together in plastic containers containing 200 ml of filtered seawater. The containers were kept at 23 [degrees]C under a light periodicity of 14L:10D for 2-5 days until fertilized eggs were obtained. Hatched planula larvae were allowed to attach to the underside of polystyrene petri dishes (9-cm diameter) floating on the water surface in the containers. The metamorphosed polyps suspended from the petri dishes were maintained at 19 or 23 [degrees]C in the dark. They were fed weekly with newly hatched Artmnia (imported from Brazil) nauplii, which were introduced into containers in excess (ca. 200-300 Anemia nauplii into 200 ml of seawater) for one day until the filtered seawater was replaced. The podocysts produced by these polyps were kept on the petri dishes along with the polyps for up to 1 year, at the two temperatures; thereafter they were kept without the polyps for various lengths of time up to 5 years, until use in this study.

Examination of the internal structure of podocysts and changes with age

To examine the internal structure of podocysts and the changes with age, eight podocysts of three different ages--less than 4 months, 18 to 20 months, and 5 years--which had been kept at 19 [degrees]C, were detached from the petri dish surface by using a blunt needle. These specimens were fixed in 2.5% glutaraldehyde in 30 mmo [l.sup.-1] HEPES buffer (pH 7.2) and kept overnight at room temperature. Fixed specimens were pierced on their lateral side using a tungsten needle to enhance the penetration of embedding medium, and were then prepared for light and electron microscopy as described below.

Preparation of excysting podocysts for histological survey

To observe the structural changes before breakage of the capsule during excystment, 40 podocysts aged less than 4 months were exposed to increased temperature (to 30 [degrees]C from 19 [degrees]C), because this temperature treatment had induced excystment efficiently (M. Kawahara, Hiroshima Univ.; pers. comm.). Five of these podocysts were detached from the dish and were fixed, at I2-h intervals over 4 days after the temperature change, with 2.5% glutaraldehyde in 30 mmol [l.sup.-1] HEPES buffer. Additionally, seven podocysts with the cell mass slightly protruding from the roof opening of the capsule were also treated with this fixative. These specimens were also prepared for light and electron microscopy as described below.

Observation of cell mass after artificial removal of the capsule

External and internal structural changes of the cell masses were observed after the capsule was artificially removed to induce them to metamorphose into polyps (Black et aL9 1976; Thein et ah, in press).

For observation of the external structure, a fine tungsten needle was used to remove the capsule from 10 podocysts with ages from 4 to 12 months. The naked cell mass was gently pipetted to a polystyrene dish (3-cm diameter) containing 3 ml of filtered seawater, and was then placed in a temperature-controlled room at 23 [degrees]C under constant darkness. The external morphology of the resulting naked cell masses was observed for about 2-3 min under a stereomi-croscope at 30 min, 1 h, 4 h, 8 h, and 24 h after the capsule was removed, and thereafter at 24-h intervals until they became polyps.

For observation of the internal structure, naked cell masses were obtained from 53 podocysts from 4 to 12 months in ape and incubated as described above. These cell masses were fixed, at various times after removal of the capsule, with 2.5% glutaraldehyde in 30 mmol [l.sup.-1] HEPES buffer and then prepared for light and electron microscopy.

Light and electron microscopy

Specimens fixed as above were postfixed with 1% osmium tetraoxide in 30 mmol [l.sup.-1] HEPES buffer (pH 7.2) for 2 h in an ice bath. Fixed samples were dehydrated using sequential ethanol solutions (50%, 70%, 90%, and 100%) and finally propylene oxide. These dehydrated samples were embedded in Quetol 651 resin (Nissin EM, Japan) at 60 [degrees]C for 24 h. For light microscopy, glass knives were used to cut sections of 500-nm thickness from the embedded samples on a Leica uc6rt ultramicrotome. Cut sections were mounted on a glass slide using heat and were stained with 0.5% toluidine blue solutions containing 0.1% borax on a heat block at 100 [degrees]C. After drying, the slides were covered by a glass slip with Enteran New (Merck, Germany) and then examined under a light microscope. For electron microscopy, sections of 80-nm thickness were cut on an ultramicrotome using a diamond knife. The cut sections were mounted on a copper grid and were then stained with 0.2%? oolong tea extract (Nissin EM, Japan) in 20 mmol [l.sup.-1] phosphate buffer (pH 7.2), followed by 0.1% Fermy's lead citrate. Thereafter, the specimens were examined using a JEOL JEM 1200 or Hitachi H-600A electron microscope.


To examine the chemical content of podocysts, five podocysts less than

4 months in age and five podocysts of 5 years in age were subjected to the histochemical staining methods described below.

The podocysts were fixed with 4% formaldehyde in 30 mmol [l.sup.-1] HEPES buffer at room temperature for 2 h. The fixed samples were dehydrated with ethanol solutions (50%, 70%, 90%, and 100%), and were embedded in LR-White resin (London Resin Company, UK) at 60 [degrees]C for 24 h. The sections (1 - [micro]m thickness) were cut using an ultramicrotome with glass knives and mounted on glass slides. These sections were examined by means of histochemical staining with the acid solochrome cyanin method for the detection of proteins (Chapman, 1968), the periodic acid Shift" (PAS) method for carbohydrates, and the methyl green and pyronin methods for nucleic acids (Al-Hazzaa and Bowen, 1998). Mayer's hematoxylin and eosin method was also applied to the sections for the examination of general morphology. The slides with stained sections were covered by a glass slip with Enteran New and were then examined under a light microscope.

For the detection of lipids, podocysts were fixed with 2.5% glutaraldehyde in 30 mmol [l.sup.-1] HEPES buffer at room temperature for 2 h and then postfixed with 1% osmium tetraoxide in 30 mmol [l.sup.-1] HEPES buffer in an ice bath for 2 h. The fixed samples were dehydrated through a series of ethanol solutions and propylene oxide as described above. Dehydrated samples were embedded in Quetol 651 resin at 60 [degrees]C for 24 h. The sections (1- [micro]m thickness) were cut on an ultramicrotome and mounted on glass slides. These sections were stained with the Sudan black B method (McGee-Russell and Smale, 1963) for the detection of lipid. As a negative control, the lipids and resin were removed from the sections with a solution of 2% potassium hydrate in ethanol (Wada et ai, 1993) and then subjected to the Sudan black B method. These slides were coated with glycerol and then covered by a glass slip and examined under a light microscope.


General structure of N. nomurai podocysts

The podocyst of Nemopilema nomurai is a dome-like capsule with a slightly concave roof and roughly oval base, in which a cell mass is encapsulated (Fig. 1). The height of the capsule ranged from 75 to 178 [micro]m (mean, 128 [micro]rn; ny 20) and the longer diameter of the basal part ranged from 184 to 471 [micro]m (mean, 320 [micro]m; n, 20). The cell mass is whitish and the capsule is slightly yellowish (Fig. 1).


Histological examination of podocysts aged less than 4 months shows that the cell mass consists of homogeneous cyst cells and sometimes has an extracellular matrix (Fig. 2A). The cyst cells have an irregular shape and are filled with many granules of various sizes (Fig. 2B, C). There are no nematocysts in the cells. The nucleus of each cell has a nucleolus (Fig. 2D). Small mitochondria occur in the cytoplasm of the cyst cells in low numbers (Fig. 2E), but neither Golgi complex nor rough endoplasmic reticulum is observed to be present.


The cyst capsule is made of chitinous cuticle (3-5 [micro]m in thickness) consisting of an outer layer composed of multiple thin lamellae (each 50-nm thick) and a single inner layer (0.2- [micro]m thick) (Fig. 3A, B). The lamellae are more densely stacked in the upper cuticle than in the lateral and bottom cuticle, so that each lamella is almost indistinguishable (Fig. 3A. C, D). The bottom cuticle undulates and has rivets projecting up into the inside of the podocyst (Fig. 3D). Beneath the bottom cuticle is an additional base layer (3--4 [micro]m in thickness) including fibrous materials that adhere to the substrate (Fig. 3D). No pores are found over the entire capsule, even under electron microscopy.


Histochemistory of podocysts

In podocysts less than 4 months old subjected to the acid solochrome cyanin method, most of the granules filling the cytoplasm of the cyst cells are stained red, indicating proteins (Fig. 4A). These granules are also stained purple using the PAS method, indicating carbohydrates (Fig. 4B). The black granules in the podocysts subjected to the Sudan black B method correspond to lipids (Fig. 4C), because they are diminished by the control treatments. Lipid granules are smaller than those of proteins and carbohydrates, and they are spread unevenly within each cell. In the methyl green and pyronin method, DNA contained in the nuclei is clearly stained purple, while the pink color indicating RNA is faint (Fig. 4D).


Histological and histochemical changes of podocysts with age

The internal structure of podocysts aged both 18 to 20 months and 5 years was not significantly different from that of podocysts less than 4 months old, both in the cell mass and in the enclosing capsule (Fig. 5A, B, C). There was no detectable difference in the ratio of cell mass volume to the inner space of cyst capsule or in the amount of extracellular matrix. Histochemical examination by means of the acid solochrome cyanin method on 5-year old podocysts demonstrated that the cell mass had been stained red, indicating proteins, as extensively as in the podocysts less than 4 months old (Figs. 4A, 5D). Even with the PAS and Sudan black B methods, the staining reactions were almost the same between the podocysts less than 4 months in age and those 5 years in age (images not shown).


Spontaneous excystment

When spontaneous excystment occurred in the laboratory, the podocysts did not show any changes in external morphology before the cell mass extruded through an opening at the roof of the cyst capsule (Fig. 6A). After the breakage of the cyst capsule, the cell mass elongated upward to become a pre-polyp form with primordial mouth and tentacles (Fig. 6B). For podocysts less than 4 months old, the duration from the breakage of cyst capsule to the development of a four-tentacle polyp was 4-7 days at 23 [degrees]C (Fig. 6C).


None of the 40 podocysts that had been exposed to increased temperature excysted during the 4-day experiment. In nine of these podocysts, the formation of nematocysts was observed in the fixed cysts (Fig. 7A, B), and in three podocysts, the cell mass was separated into ectoderm and endoderm, forming a stratified structure (Fig. 7C, D). The remaining 28 podocysts did not show any changes in internal structure from the dormant form.

In podocysts with the cell mass just slightly extruding through the opening on the upper side of the capsule, the cell mass was completely stratified and the ectoderm cells had lost the granules in their cytoplasm (Fig. 7E). A gap occurred in the central part of the endoderm, and the extracellular matrix had disappeared (Fig. 7E). At the same time, the ectoderm cells near the opening had many vesicles in their cytoplasm (Fig. 7F). The outer layer of the upper side of the capsule disappeared, but the inner layer remained (Fig. 7E, F). The cell mass then extruded farther beyond the opening, with the invagination of ectoderm uppermost (Fig. 7G), and the inner layer of the capsule was broken at the opening area (Fig. 7H).

Artificial metamorphosis by capsule removal

In the 10 stripped podocysts whose capsules were artificially removed, the naked cyst cells adopted a spherical shape with a smooth surface within 30 min, even though they had been damaged in the process of manually removing the capsule (Fig. 8A, B). Two to five days after capsule removal, the cell mass elongated and began to form a primordial mouth and tentacles (Fig. 8C). Thereafter, the aboral end of the cell mass extended to form a peduncle and pedal disc to attach to the substrate, and metamorphosis into a four-tentacle polyp was completed in 3 to 6 days, with one exception of 30 days, after the capsule was removed (Fig. 8D). In this artificial capsule removal experiment, all 10 of the podocysts less than 4 months old successfully metamorphosed into polyps.


On the basis of histological examination of the cell mass after capsule removal, the process of metamorphosis can be divided into five stages. The first stage is a naked cell mass bearing no nematocysts (Fig. 9A); in the second stage, nematocysts are formed extensively within the cell mass (Fig. 9B, C); in the third stage, the cell mass stratifies into ectoderm and endoderm (Fig. 9D); in the fourth stage, the cell mass elongates with the ectoderm invaginating into the inner part at one end, forming a primordial mouth and tentacles (Fig. 9E); in the fifth (final) stage, the cell mass completes metamorphosis into a polyp with elongated peduncle, pedal disc, tentacles, epithelium, and a coelenteron (Fig. 9F).


Figure 10 summarizes the temporal shift of the above-mentioned five stages for the cell mass specimens after the capsule was removed. The first-stage cell mass remained for up to 48 h after capsule removal. Some of the stripped podocysts developed into advanced stages immediately after capsule removal, and there were cases where the third-stage form had developed within the first hour. However, more typically, metamorphosis progressed to the advanced stages later than 48 h after capsule removal. The first polyp (or the fifth-stage form) appeared 24 h after capsule removal, although it generally took 5-6 days for most of the stripped podocysts to metamorphose into polyps.



Morphological features of dormant podocysts

The morphological features of the laminated structure of the capsule and a nutrient-rich dormant cell mass in the podocysts of Nemopilema nomurai are also common to the podocysts of the semaeostome species Aurelia aurita (Chapman, 1968; Thein et al, in press), Chrysaora quinquecirrha (Blanquet, 1972; Black et al, 1976), and Cyanea lamarcki [as C. palmstruchi] (Widersten, 1969). The capsule is probably made of a chitin-protein complex tanned by a phenolic oxidase, as has been reported for C. quinquecirrha (Blanquet, 1972), and its thick outer layer may be chemically resistant against infestation by bacteria and fungi (Blanquet, 1972), as well as physically robust to avoid predation by nudibranchs (Cargo and Shultz, 1967) or other animals. The inner capsule layer may be formed by the cyst cells after the formation of the outer layer, as has been observed for A. aurita podocysts (Chapman, 1968; Thein et al., in press). The structure of the base layer of the cyst capsule of N. nomurai (Fig. 3D) is the same as that of the basal cuticle beneath the pedal disc of A. aurita polyps, which form podocysts above the basal cuticle of the pedal disc (Chapman, 1968, 1969), indicating that the capsule of TV. nomurai podocysts is also formed above the basal cuticle of polyps.

The storage of proteins, carbohydrates, and lipids in the dormant cell mass of N. nomurai podocysts is also the same as in A. aurita (Chapman, 1968; Thein et al, in press), C. quinquecirrha (Black et al.9 1976), and Cyanea lamarcki [as C. palmstruchi] (Widersten, 1969). These compounds are stored in the granules of the cyst cells (Figs. 2 and 4). Our histochemical observations revealed that proteins and carbohydrates are stored in the same granules, while lipids are stored in different, smaller granules (Fig. 4). This may indicate different usage of these nutrient reserves during dormancy and excystment.

Of the 13 dormant N. nomurai podocysts examined, we found no nematocysts in any of them. However, nematocysts are commonly borne in the podocysts of the three semaeostome species that have been studied (Chapman, 1968; Widersten, 1969; Black, 1981; Thein et al, in press). Nematocysts are the cellular organelles used for capture of prey when podocysts become polyps (Lesh-Laurie and Suchy, 1991; Kass-Simon and Scappaticci, 2002), and are therefore unnecessary during podocyst dormancy. Perhaps N. nomurai podocysts maximize nutrient-reserve storage for dormancy in lieu of nematocyst possession. However, it remains to be studied whether dormant podocysts of other rhizostome species are also devoid of nematocysts.

The extracellular matrix in N. nomurai podocysts (Fig. 2A), which appears to be identical to the central clear zone in A. aurita podocysls (Chapman, 1970), may be made from polyp mesoglea pinched off by the cyst cells, as described in C. lamarcki [as C. palmstruchi] (Widersten, 1969) and A. aurita (Chapman, 1970). The mesogleal extracellular matrix has been shown to play a role in maintaining the shape of polyps and medusae (Chapman, 1953), and it may therefore have the same function in the cell mass of the podocysts.

Structural aspects of dormancy

Mitochondria, Golgi complex, and rough endoplasmic reticulum are very scarce in the cells of N. nomurai podocysts (Fig. 2C, D, E). This scarcity, in addition to the weak reaction for RNA in the methyl green and pyronin method (Fig. 4D), suggests that the dormant podocysts have low respiration and protein synthesis rates in spite of their rich nutrient reserves. Similar properties have been demonstrated in the podocysts of A. aurita (Chapman, 1968; Thein et al, in press) and C. quincuecirrha (Black, 1981). Surprisingly, our histochemical examinations did not demonstrate any significant difference in the ratio of cell mass volume to the inner space of cyst capsule or in the reaction for nutrient reserves between newly produced (i.e., Less than 4-month-old) and 5-year-old podocysts (Fig. 5). In A. aurita podocysts, however, the cell mass decreased its volume to almost half of the initial one after 12 months of dormancy, and their maximum longevity was 3.2 years (Thein et al, in press). Furthermore, Black (1981) reported that C. quinquecirrha podocyts lost half of the DNA, one-third of the proteins, and one-fifth of the lipids contained in newly formed podocysts during the first year. The deep dormancy with extremely low metabolic activity in N. nomurai podocysts is distinctive, and may explain how this species is able to maintain dormancy for much longer periods than A. aurita.

Low metabolic activity is suggested to be an advantage for tolerance of anaerobic conditions (Guppv and Withers, 1999). A. aurita podocysts can survive under hypoxia (0.2-1.0 mg [O.sub.2] l (-1) for 12 days and maintain the ability of excystment (Thein el al, in press). Similar tolerance against hypoxia, as well as to burial under organic-rich silty mud, has also been observed for N. nomurai podocysts in the laboratory (M. Kawahara, Hiroshima Univ.; pers. comm.). Extremely low metabolism of the dormant cells combined with physicochemical strength of the enclosing capsule may allow the podocysts of N. nomurai to minimize mortality and increase their longevity.

The metamorphosis process in excystment

In our examination of spontaneous excystment, the podocysts first began formation of nematocysts in the cell mass, followed by stratification of endoderm and ectoderm, prior to extrusion of the cell mass from the capsule (Fig. 7A-D). The morphogenesis of the cell mass is largely similar to embryogenesis from an egg, through a planula larva, to a polyp (Kawahara et al. 2006; Yuan et al., 2008). In particular, the stratified cell mass resembles a planula (Yuan et al., 2008), indicating that the podocyst cell mass develops through a planula-like form before metamorphosis into a polyp. Upon breakage of the cyst capsule, the outer cuticle layer is decomposed, probably by enzymes (e.g., chitinase and protease) secreted from the cells adjacent to the roof (Fig. 7E, F); the inner layer is then torn, perhaps mechanically by the pushing up of the extruding cell mass (Fig. 7G, H). These processes suggest some chemical differences between the two layers.

Both the external and internal changes to the cell mass of artificially stripped N. nomurai podocysts are basically the same as those observed in spontaneous excystment (Fig. 6-9), as has already been described in C. quinquecirrha podocysts (Black et al., 1976). Early-developing cell masses in the third to fifth stages within 24 h after capsule removal may have already started metamorphosing before the treatment (Fig. 10). On the basis of the integrated information from these processes of metamorphosis (Figs. 7, 9, 10), we assume that the following process occurs during the excystment of podocysts: (1) formation of nematocysts after the breakage of dormancy, (2) stratification of the cell mass into ectoderm and endoderm, (3) dissolution of the outer layer of capsule, (4) extrusion from the opening and formation of primordial polyp mouth and tentacles, and (5) completion of metamorphosis into a polyp.

Role of podocysts for medusa blooms

Podocysts have two major ecological roles in the life cycle of N. nomurai: one is the asexual reproduction by which the polyps increase their numbers (Kawahara et al., 2006), and the other is the dormancy by which the population can perpetuate for longer periods by tolerating unfavorable environmental conditions such as hypoxia, low prey availability, and predator existence (M. Kawahara, Hiroshima Univ.; pers. comm.). Hence, the performance of podocysts (e.g., maintaining dormancy or excystment into polyps) must be an important factor in determining the population abundance of N. nomurai medusa in the following seasons.

Our histological and histochemieal study confirms that N. nomurai podocysts are capable of long dormancy (Fig. 5), and are therefore able to accumulate in the coastal waters of the Yellow and East China Seas, the seeding and nursery ground for this species, over several years. If the accumulated podocysts are exposed to some environmental factor, such as an increase in temperature, that induces excystment, the polyp abundance may greatly increase, leading to the liberation of large numbers of medusae and a massive bloom. Although increased human impacts to the coastal marine ecosystem have been argued to be the primary environmental causes for the recurrent N. nomurai blooms (Uye, 2008, 2011), this study suggests that the physioecological specificities of the podocysts should also be taken into consideration to understand the mechanisms of the blooms, especially for the remarkable year-to-year variations in the magnitude of the bloom intensity.


We thank M. Kawahara (Hiroshima University) and M. Nishizaki (Shimane University) for assistance with the collection of jellyfish and with experiments, and K. Koike (TEM service, Hiroshima University) for help with transmission electron microscopy. We also thank C. Mills (University of Washington) for editing our manuscript and for helpful comments. This research was supported by research grants from the Japan Society for the Promotion of Science (No. 20780138) and the Ministry of Agriculture, Forestry, and Fisheries of Japan.

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(1.) Graduate School of Biosphere Science, Hiroshima University, 4-4, Kagamiyama I Chome, Higashi-Hiroshima, 739-8528, Japan; and (2.) Oki Marine Biological Station, Faculty of Life and Environmental Science, Shimane University, 194 Kamo, Okinoshima-cho, Oki 685-0024, Japan

Received 25 August 2011; accepted 20 October 2011.

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Author:Ikeda, Hideki; Ohtsu, Kohzoh; Uye, Shin-Ichi
Publication:The Biological Bulletin
Article Type:Report
Geographic Code:9JAPA
Date:Dec 1, 2011
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