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Timing of spawning and early development of Palythoa tuberculosa (Anthozoa, Zoantharia, Sphenopidae) in Okinawa, Japan.

Introduction

Zoantharia (Cnidaria, Anthozoa, Hexacorallia) is an order of benthic cnidarians. and zoanthid species are widespread globally from the intertidal zone to the deep sea. They are characterized by (1) a distinctive arrangement of radially disposed septa (= mesenteries) and two rows of tentacles; (2) the lack of skeleton (except for the genus Savalia), with most species incorporating sand grains into their tissue; (3) a distinctive, modified planula larva, either "zoanthella" or "zoanthina." Zoanthids, with exception of the solitary Sphenopus, generally form clonal aggregations or colonies. They are often an abundant component of marine communities, particularly in tropical ecosystems (see Fadlallah et al., 1984). Despite its ecological and phylogenetic importance, this taxon has been the subject of few studies on its reproductive biology (reviewed by Ryland, 1997), probably because of its confused taxonomy (Burnett et al., 1997; Reimer et al., 2004) and difficulty in internal observation due to sand encrustation (Reimer et al., 2010).

The order Zoantharia (=Zoanthidea) is divided into two suborders by arrangement of their mesenteries. Colonies in the suborder Macrocnemina are, with few exceptions, gonochoric. On the other hand, colonies are commonly hermaphroditic in the suborder Brachycnemina, which includes the genera Palythoa and Protopalythoa, although small samples may yield only unisexual polyps (Ryland, 1997). Shallow-water zoanthids ranging from higher latitudes (54-61[degrees]N) to tropical areas often have annual cycles of gametogenesis (see Ryland, 1997, 2000), while Epizoanthus species in deep water breed continuously (Muirhead et al., 1986). To date, there have been a few reports on the spawning behavior of zoanthids in the laboratory (Kimura et al., 1972) and in the field (Ryland and Babcock et al., 1991). and internal brooding has been confirmed only in Isozoanthus giganteus (mentioned in Ryland, 1997).

Two types of larvae have been reported for zoanthids. The zoanthella larva (named by van Beneden, 1897) was first described by Semper (1867); this larva is an almost cylindrical planula that has a long, mid-central ciliary band extending from the blastopore to the anterior pole. Semper's "second" larva, designated the zoanthina larva (named by van Beneden, 1897), has a spherical or somewhat elongated body with an equatorial ciliary band. Menon (1902, 1914, 1926) revealed that the genera Sphenopus and Protopalythoa (family Sphenopidae) produce zoanthella, and the genera Isaurus and Zoanthus (family Zoanthidae) produce zoanthina. Kimura et al. (1972) later reported that Palythoa (Sphenopidae) also produces zoanthella. Most descriptions of zoanthid larvae have been based on specimens collected with plankton tows (Menon. 1902; Scheltema, 1971; Nielsen. 1984), and species identification of the larvae has often been impossible. Babcock and Ryland (1990) raised the fertilized eggs of Protopalythoa sp. to zoanthella larvae, and to date this is the only description of zoanthid development from spawning to settlement.

Species of the genus Palythoa are colonial, generally zooxanthellate, and commonly found in shallow coral reefs worldwide. Recent studies using sequences of the internal transcribed spacer of ribosomal DNA (ITS-rDNA) from Palythoa specimens in Japan have suggested that the very closely related Palythoa species "liberae" Palythoa mutuki, "immersae" P. tuberculosa, and "intermediate morphology" Palythoa sp. have experienced reticulate evolution (Reimer et al., 2007a). However, there is little information about sexual reproduction of Palythoa spp. in Japan: (1) P. tuberculosa produces gametes in summer (Yamazato et al., 1973; Shiroma and Reimer, 2010); and (2) eggs were observed to be released from laboratory-cultured colonies in August and developed into zoanthellae (Kimura et al., 1972).

In August 2009, we observed natural spawning of Palythoa tuberculosa Klunzinger, 1877 in the field and the release of zygotes that developed into zoanthellae. Here, we report on the embryology and fine structure of zoanthella larvae of P. tuberculosa.

Materials and Methods

Collection and observation of early development

In Okinawa. Palythoa tuberculosa often forms large aggregations, consisting of many colonies, in the intertidal and shallow subtidal zones. Released zygotes of P. tuberculosa from a large aggregation (up to 4 [m.sup.2]) were collected by scuba at Mizugama, on the west coast of Okinawa Island, Japan (26[degrees]21'38 N, 127[degrees]44'20 E) on 19 and 20 August 2009. Released zygotes were caught in situ and brought to the laboratory in 300-ml plastic bottles filled with seawater. A few colonies were collected from the same aggregation at the same time and fixed with 10% formalin-seawater.

Embryos and larvae were reared in 200-ml plastic jars filled with 0.45-[micro]m-pore filtered seawater (FSW) at room temperature (27-29 [degrees]C), and FSW was changed daily. The embryos and larvae were observed under a light microscope, and photomicrographs were taken.

Microscopy

Embryo and larvae were fixed in 2.5% glutaraldehyde in FSW and stored at 4 [degrees]C. Specimens were then rinsed with 0.1 mol [l.sup.-1] cacodylate-0.45 mol [l.sup.-1] sucrose and post-fixed in 1% osmium tetroxide-0.1 mol [l.sup.-1] cacodylate for 2 h. After dehydration through a graded ethanol series, some specimens were immersed in t-butanol, freeze-dried, sputter-coated with gold-palladium, and examined under a scanning electron microscope (SEM: JEOL JSM-6060LV) at low vacuum mode (backscattered electron images at about 30 Pa). Other specimens were immersed in n-butyl glycidyl ether and embedded in epoxy resin (Quetol 812, Nissin EM). Sections of 0.5-1 [micro]m thick were stained with toluidine blue for light microscopy. Thin sections were stained with lead citrate and uranyl acetate and examined with a transmission electron microscope at 80 kV (TEM: JEOL JEM-1011).

Results

Observation of spawning

Some polyps of Palythoa tuberculosa had no gonads, and some developed either testes or ovaries (Fig. 1 A); no polyp was hermaphroditic. Zygote spawning of P. tuberculosa was observed between 2030 and 2200 h on both 19 and 20 August 2009 at a shallow reef. P. tuberculosa spawned just after high tide on new moon nights (Fig. 1D). We confirmed that several colonies within the same aggregation released their zygotes on both days. However, we do not know whether colonies are clones or genetically different colonies because individual-level genetic markers do not yet exist for zoanthids. The zygotes (fertilized eggs) were released through the mouth as tightly packed clusters. Packed zygotes (fertilized egg bundles) were highly buoyant (Fig. 1B, C). The diameter of packed zygotes was 2-3 mm. Zygote spawning was not strictly synchronized within and among colonies. The zygotes were orange and did not contain any symbiotic microalgae (zooxanthellae). The diameter of zygotes was 365.6 [+ or -] 14.8 [micro]m (average [+ or -] SD) (Fig. 2A). We did not see the release of sperm during the observation period. However, the collected egg bundle, containing potentially fertilized eggs ( = zygotes), began to develop (see Discussion).

[FIGURE 1 OMITTED]

[FIGURE 2 OMITTED]

Embryogenesis of P. tuberculosis

About 2 h after spawning, the first cleavage furrow appeared on one side of the zygotes, producing a heart-shaped cleavage stage (Fig. 2B). The first cleavage was equal and holoblastic (Fig. 2C). After the second cleavage, the arrangement of blastomeres was pseudospherical (Fig. 2D), but subsequent cleavages appeared to be less regular, resulting in cells of different sizes (Fig. 2E-I). Cleavage occurred at intervals of 30-45 min. At 9 h after spawning, embryos consisted of a bilayer of cells with no definite blastocoel. The embryos then became concave-convex dish-shaped (Fig. 3A, B, C). At 12 h after spawning, embryos were roughly spherical, with a blastopore (Fig. 3D, E, F). At 24 h after spawning, the surface of embryos became smooth, and the spherical larvae crept along the bottom of the plastic jar (Fig. 3G, H). At this stage, the blastopore was closed and there was no coelenteron (= gastrovascular cavity) observed in histological examination (Fig. 31). Seven-day-old larvae were ellipsoid and about 700 [micro]m long and 350 [micro]m wide, with an anterior, open mouth (Fig. 3J). The surfaces of larvae were slightly concave, and a shallow groove formed a line along the long axis (Fig. 3K, arrowhead). At this stage, the body of the larvae consisted of two germ layers (ectoderm and endoderm) that were separated by the mesoglea. Ectodermal cells were columnar and stained weakly with toluidine blue, while endodermal cells were irregularly shaped and highly vacuolated due to lipid storage (Fig. 3L, M). At the mouth opening, the ectoderm turned inward to form a ciliated lining of the mouth. The mouth lumen was continuous with the coelenteron that was lined with endoderm (Fig. 3L). A cross section of the concave groove in a 7-day larva showed that ciliary bundles emerged from the bottom of the shallow groove (Fig. 3N). Larvae rotated on the oral-aboral axis and swam in an aboral direction, regardless of the movement of the cilia.

Zoanthella larvae of P. tuberculosa

About 13 days after spawning, larvae developed a longitudinal band of long cilia (= ventral ciliate band) that is characteristic of zoanthella larvae (Fig. 4A). The longitudinally enlarged band moved rhythmically right and left along the oral-aboral axis in a coordinated wave-like fashion. However, the larva rotated on the oral-aboral axis with the enlarged ciliate band. The enlarged band appeared not to play a major role in the locomotion of larvae, as it occasionally stopped but the larvae continued to move. At this stage, a pharynx with six mesenteries was formed (Fig. 4B, C, D), although only two mesenteries were observed in the posterior half of the larvae (Fig. 4E). At 22 days after spawning, several nematocysts were found in the ectoderm, and the larvae still contained many lipid drops in the endodermal layer (Fig. 4F). Each cell of the ventral ciliate band carried one cilium and one microvillus (Fig. 4G, inset). Each cilium was associated with an accessory centriole and striated ciliary root. Septate junctions were found at the latero-distal part of the ectodermal cells (Fig. 4G).

Discussion

Shallow-water zoanthids have been shown to have annual cycles of gametogenesis: Zoanthus spp. and Palythoa caribaeorum in the North Atlantic and Caribbean (Karlson, 1982; Fadlallah et al., 1984), Zoanthus pacificus and Palythoa vestitus in Hawaii (Cooke, 1976), Protopalythoa sp. in the Great Barrier Reef (GBR) (Ryland and Babcoek, 1991), Palythoa caribaeorum and Protopalythoa variabilis in Brazil (Boscolo and Silveira, 2005), and Zoanthus sansibaricus in Kagoshima, Japan (Ono et al., 2005). However, there are few reports about timing and mode of spawning events in zoanthids. In the GBR, Protopalythoa sp. was confirmed both by field and laboratory observations to release gametes three to five nights (from 1930 to 2200 h) after the full moon in early summer (November) (Babcock and Ryland, 1990; Ryland and Babcock, 1991). In Bermuda, a major spawning of Parazoanthus parasiticus was inferred through histological study to occur one to two nights after the full moon in summer (September) (Ryland, 1997). Kimura et al. (1972) reported that Palythoa tuberculosa released its eggs in August in the laboratory in Okinawa; however, they did not describe the exact day or time of the spawning. In the temperate zone of Japan, Zoanthus sansibaricus spawning was estimated through histological study to occur three to five nights after the full moon in summer (July) (Ono et al., 2005).

In this study we observed the spawning behavior of P. tuberculosa one day before and on the night of the new moon in mid-summer (August) in the field. In the Okinawa Islands, most scleractinian corals release their gametes around full moon nights during the summer (June to August) (Heyward et al., 1987; Richmond, 1997). Pocillopora verrucosa (Hirose et al., 2000) and Fungia repanda (Loya et al., 2009) release their gametes a few days after new moon mornings (spawn at 0600-0700 and 0300-0500, respectively), but there are no reports of corals spawning around new moon nights in Okinawa. This is the first report of new moon night spawning in either scleractinian corals or zoanthids in Okinawa. The seasonal reproduction patterns and the timing of gamete release in hexacorals are influenced by various factors--for example, temperature, salinity, food availability, moon phases, and tides--but it is unclear how these factors may interact in series of complex events (Jokiel et al., 1985; Harrison and Wallace, 1990; Perse et al., 1991; Richmond, 1997). The spawning behavior of Protopalythoa sp. on the GBR was observed at about the same time as scleractinian coral mass spawning there (Babcock and Ryland, 1990; Ryland and Babcock, 1991), while the spawning of P. tuberculosa is not synchronized with scleractinian corals in Okinawa. The cue or cues for P. tuberculosa spawning may be different from those for both Protopalythoa sp. on the GBR and for most scleractinian corals in Okinawa.

Traditionally, the identification of Palythoa species has been based on morphological characters such as polyp shape and size, colony color, as well as locality and habitat (see Ryland and Lancaster, 2003). However, species diversity, identification, and taxonomy within the genus Palythoa remain very difficult and confused, as Palythoa species are distributed worldwide and show large intraspccific variations in morphology (Muirhead and Ryland, 1985; Ryland and Muirhead, 1993; Burnett et al., 1994, 1997). The present study demonstrated the timing and mode of spawning and embryogenesis of P. tuberculosa. The results of this study will help to examine whether reproductive isolation exists among P. tuberculosa, P. mutuki, and Palythoa sp., which are implicated in reticulate evolution by DNA molecular analyses (Reimer et al., 2007a, b), and exist sympatrically on coral reefs in southern Japan.

The eggs of Protopalythoa sp. on the GBR were 300 [micro]m in diameter and contained symbiotic algae (zooxanthellae) (Babcock and Ryland, 1990). In contrast, P. tuberculosa zygotes in Okinawa were about 365 [micro]m in diameter and did not contain zooxanthellae. However, the patterns of early embryogenesis, especially modes of gastrulalion, are very similar in both species. This gastrulation pattern is similar to that of Acropora spp. (Anthozoa, Scleractinia, Cnidaria) (Miller and Ball, 2000; Okubo and Motokawa, 2007) and is very unique. In addition, both zoanthellae larvae appeared at 2 weeks after spawning. Recently, Reimer et al. (2006, 2007a) demonstrated by DNA phylogenetic analyses that the genus Palythoa should include both Palythoa species and species formerly assigned to the genus Protopalythoa. The similarity of early embryogenesis and larval types supports the results of these molecular phylogenetic analyses.

Babcock and Ryland (1990) confirmed that three types of gamete release occur simultaneously in one Protopalythoa species on the GBR--egg-sperm bundles, egg bundles without sperm, and freely shed sperm--and they then observed early embryogenesis of this species. However, it is impossible to ascertain when gametes of Protopalythoa sp. were fertilized, because the authors did not describe natural or artificial fertilization of their samples. In this study, we confirmed the presence of mature testes in colonies at spawning time, but we did not observe freely shed sperm or egg-sperm bundles in the field. However, most "eggs" that were captured from the water column began to cleave within 2 h after spawning. It is possible that "eggs" were fertilized in the gastric cavity before release as an "egg bundle," or that they were fertilized in the water column by a very dilute concentration of sperm. In scleractinian corals, most spawning species release their gametes simultaneously and fertilization takes place in the water column or at the water surface within hours (Harrison and Wallace, 1990). The mode of sexuality and the spawning behavior of zoanthid species appear to be rich in variety and different from those of scleractinian corals.

Acropora is one of the most speciose and widely distributed scleractinian corals (Veron and Wallace, 1984), and the egg diameters of Acropora spp. are 300-400 [micro]m (Harrison and Wallace. 1990). comparable to those of Protopalythoa sp. (Babcock and Ryland, 1990; Ryland and Babcock, 1991) and P. tuberculosa (this study). Most Acropora larvae settle on substrate within 9-10 days after spawning under experimental conditions (Nozawa and Harrison, 2008), and these larvae settle mainly within a local population (e.g., Ayer and Hughes, 2000; Nishikawa and Sakai, 2005; Nakajima et al., 2009, 2010; Hemond and Vollmer, 2010). On the other hand, it takes more than 2 weeks for Protopalythoa sp. (Babcock and Ryland, 1990) and P. tuberculosa (this study) to develop mature, motile zoanthella larvae. Palythoa spp. (including genus Protopalythoa) are widespread in the subtropical and tropical zones, and molecular phylogenetic analyses have shown the number of species to be much less than previously assumed, also with potentially much lower levels of local endemism than previously believed (Burnett et al., 1997; Reimer et al., 2006, 2007a; Reimer and Hickman, 2009). A long floating, planktonic period may be one reason for the wide distribution ranges and low endemism in Palythoa spp.

Cnidarians are generally regarded as having a radially symmetrical body plan with a single major axis of polarity, the oral-aboral axis. In most anthozoans, a radial polypoid stage starts alter larvae settle on substrate and metamorphose into primary polyps. The shape of planula larvae is cylindrical with a radially symmetrical body plan, but some gene expression patterns indicate that planula larvae are asymmetrical along an axis perpendicular to the oral-aboral axis, the directive axis (Hayward et al., 2002; Finnerty et al., 2004; Matus et al., 2006a, b; Rentzsch et al., 2006; Saina et al., 2009). Thus, the common ancestor of Cnidaria may have had a bilateral body, which was secondarily lost in non-bilateral cnidarians (the Medusozoa) (see Manuel, 2009). Recent morphological and molecular phylogenetic evidence indicates that the class Anthozoa is the most basal group in the extant cnidarians (Bridge et al., 1992, 1995; Odorico and Miller. 1997; Kim et al., 1999; Medina et al., 2001). Anthozoa is divided into two subclasses (Hexacorallia and Octocorallia), and recent molecular phylogenic analyses show that Actinaria or Zoantharia (or both) are the most ancestral group within extant Hexacorallia species (Medina et al., 2006; Brugler and France, 2007; Sinniger et al., 2007; Fukami et al., 2008: Sinniger and Pawlowski. 2009). Both polypoid and larval stages of zoanthid internal structures display biradial symmetry (see Ryland et al., 2000). and zoanthella larvae have a cililate band along the oral-aboral axis. Expression patterns of axis-related genes, such as Dpp/BMP and chording/sog, and their functional analyses should be examined in zoanthella larvae to clarify the regulation and determination of the axes and body plans in primitive Radiata.

Acknowledgments

We thank Mr. Takuma Fujii (University of the Ryukyus) for held help. J.D.R. was supported in part by the Rising Star Program at the University of the Ryukyus, and by a Japan Society for the Promotion of Science "Wakate B" (#21770089) grant-in-aid.

Literature Cited

Ayre, D. J., and T. P. Hughes. 2000. Genotypic diversity and gene flow in brooding and spawning coral along the Great Barrier Reef. Australia. Evolution 54: 1590-1605.

Babcock, R. C, and J. S. Ryland. 1990. Larval development of a tropical zoanthid (Protopalythoa sp.). Invertebr. Reprod. Dew 17: 229-236.

Boscolo, H. K., and F. L. Silveira. 2005. Reproductive biology of Palythoa caribaeorum and Protopalythoa variabilis (Cnidaria. Anthozoa, Zoanthidea) from the southeastern coast of Brazil. Braz. J. Biol. 65: 29-41.

Bridge, D., C. W. Cunningham, B. Schierwater, R. DeSalle, and L. W. Buss. 1992. Class-level relationships in the phylum Cnidaria: evidence from mitochondrial gene structure. Proc. Natl. Acad. Sci. USA 89: 8750-8753.

Bridge, D., C. W. Cunningham. R. DeSalle, and L. W. Buss. 1995. Class-level relationships in the phylum Cnidaria: molecular and morphological evidence. Mol. Biol. Evol. 12: 679-689.

Brugler, M. R., and S. C. France. 2007. The complete mitochondrial genome of the black coral Chrysopathes formosa (Cnidaria: Anthozoa: Antipatharia) supports classification of antipatharians within the subclass Hexacorallia. Mol. Phylogenet. Evol. 42: 776-788.

Burnett, W. J., J. A. H. Benzie, J. A. Beardmore, and J. S. Ryland. 1994. High genetic variability and patchiness in a common Great Barrier Reef zoanthid (Palythoa caesia). Mar. Biol. 121: 153-160.

Burnett, W. J., J. A. H. Benzie. J. A. Beardmore, and J. S. Ryland. 1997. Zoanthids (Anthozoa, Hexacorallia) from the Great Barrier Reef and Torres Strait. Australia: systematics, evolution and a key to species. Coral Reefs 16: 55-68.

Cooke, W. J. 1976. Reproduction, growth and some tolerances of Zoanthus pacificus and Palythoa vestitus in Kaneohe Bay. Hawaii. Pp. 281-288 in Coelenterate Ecology and Behaviour. G. O. Mackie. ed. Plenum Press, New York.

Fadlallah, Y. H., R. H. Karlson, and K. P. Sebens. 1984. A comparative study of sexual reproduction in three species of Panamanian zoanthids (Coelenterata: Anthozoa). Bull. Mar. Sci. 35: 80-89.

Finnerty, J. R., K. Pang, P. Burton, D. Paulson, and M. Q. Martindale. 2004. Origins of bilateral symmetry: Hox and dpp expression in a sea anemone. Science 304: 1335-1337.

Fukami, H., C. A. Chen, A. F. Budd, A. Collins, C. Wallace, Y. Y. Chuang, C. Chen, C. F. Dai, K. Iwao, C. Sheppard, and N. Knowlton. 2008. Mitochondrial and nuclear genes suggest that stony corals are monophyletic but most families of stony corals are not (order Scleractinia, class Anthozoa, phylum Cnidaria). PLoS ONE 3: e3222.

Harrison P. L., and C. C. Wallace. 1990. Reproduction, dispersal and recruitment of seleractinian corals. Pp. 133-107 in Ecosystems of the World. 25. Coral Reefs, Z. Dubinsky. ed. Elsevier. Amsterdam.

Hayward, D. C, G. Samuel, P. C. Pontynen, J. Catmull, R. Saint, D. J. Miller, and E. E. Ball. 2002. Localized expression of a dpp/BMP2/4 ortholog in a coral embryo. Proc. Natl. Acad. Sci. USA 99: 8106-8111.

Hemond, E. M., and S. V. Vollmer. 2010. Genetic diversity and connectivity in the threatened staghorn coral (Acropora cervicornis) in Florida. PLoS ONE 5: e8652.

Heyward, A., K. Yamazato, T. Yeemin, and M. Minei. 1987. Sexual reproduction of corals in Okinawa. Galaxea 6: 331-343.

Hirose, M., R. A. Kinzie, and M. Hidaka. 2000. Early development of zooxanthella-containing eggs of the corals Pocillopora verrucosa and P. eydouxi with special reference to the distribution of zooxanthellae. Biol. Bull. 199: 68-75.

Jokiel, P. L., R. Y. Ito, and P. M. Liu. 1985. Night irradiance and synchronization of lunar release of planula larvae in the reef coral Pocillopora damicornis. Mar. Biol. 88: 167-174.

Karlson, R. H. 1982. Reproductive patterns in Zoanthus spp. from Discovery Bay, Jamaica. Pp. 699-704 in Proceedings of the 4th International Coral Reef Symposium. Vol. 2. E. D. Gomez, C. E. Birkeland, R. W. Buddemeier, R. E. Johannes, J. A. Marsh. Jr.. and R. T. Tsuda, eds. Marine Science Center. University of the Philippines. Manila.

Kim, J., W. Kim, and C. W. Cunningham. 1999. A new perspective on lower metazoan relationships from 18S rDNA sequences. Mol. Biol. Evol. 16: 423-427.

Kimura, S., Y. Hashimoto, and K. Yamazato. 1972. Toxicity of the zoanthid Palythoa tuberculosa. Toxicon 10: 611-617.

Loya, Y., K. Sakai, and A. Heyward. 2009. Reproductive patterns of fungiid corals in Okinawa, Japan. Galaxea 11: 119-129.

Manuel, M. 2009. Early evolution of symmetry and polarity in metazoan body plans, C. R. Biol. 332: 184-209.

Matus, D. Q., G. H. Thomsen, and M. Q. Martindale. 2006a. Dorso/ ventral genes are asymmetrically expressed and involved in germ-layer demarcation during cnidarian gastrulation. Curr. Biol. 16: 499-505.

Matus, D. Q., K. Pang, H. Marlow, C. W. Dunn, G. H. Thomsen, and M. Q. Martindale. 2006b. Molecular evidence for deep evolutionary roots of bilaterality in animal development. Proc. Natl. Acad. Sci. USA 103: 11195-11200.

Medina, M., A. G. Collins, J. D. Silberman, and M. L. Sogin. 2001. Evaluating hypotheses of basal animal phylogeny using complete sequences of large and small subunit rRNA. Proc. Natl. Acad. Sci. USA 98: 9707-9712.

Medina, M., A. G. Collins, T. L. Takaoka, J. V. Kuehl, and J. L. Boore. 2006. Naked corals: skeleton loss in Scleractinia. Proc. Natl. Acad. Sci. USA 103: 9096-9100.

Menon, K. R. 1902. Notes on Semper's larvae. Proc. Cambridge Philos. Soc. 11: 407-417.

Menon, K. R. 1914. Preliminary note on the metamorphosis of Zoan-thella. Rec. Indian Mus. 10: 212-213.

Menon, K. R. 1926. On the adults of Zoanthella and Zoanthina, Rec. Indian Mus. 28: 61-64.

Miller, D. J., and E. E. Ball. 2000. The coral Acropora: what it can contribute to our knowledge of metazoan evolution and the evolution of developmental processes. Bioessays 22: 291-296.

Muirhead, A., and J. S. Ryland. 1985. A review of the genus Isaurus Gray 1828 (Zoanthidea),. including new records from Fiji. J. Nat. Hist. 19: 323-335.

Muirhead, A., P. A. Tyler, and M. H. Thurston. 1986. Reproductive biology and growth of the genus Epizoanthus (Zoanthidea) from the north-east Atlantic. J. Mar. Biol. Assoc. UK 66: 131-143.

Nakajima, Y., A. Nishikawa, N. Isomura, A. Iguchi, and K. Sakai. 2009. Genetic connectivity in the broadcast-spawning coral Acropora digitifera analyzed by microsatellite markers on the Sekisei Reef, Southwestern Japan. Zool. Sci. 26: 209-215.

Nakajima, Y., A. Nishikawa, A. Iguchi, and K. Sakai. 2010. Gene flow and genetic diversity of a broadcast-spawning coral in northern peripheral populations. PLoS ONE 5: e11149.

Nielsen, C. 1984. Notes on a Zoanthina larva (Cnidaria) from Phuket, Thailand. Vidensk. Medd. Dan. Nathist. Foren. 145: 53-60.

Nishikawa, A., and K. Sakai. 2005 Settlement-competency period of planulae and genetic differentiation of the scleractinian coral Acropora digitifera. zool Sci. 22: 391-399.

Nozawa, Y., and P. L. Harrison. 2008. Temporal patterns of larval settlement and survivorship of two broadcast-spawning acroporid corals. Mar. Biol. 155: 347-351.

Odorico, D. M., and D. J. Miller. 1997. Internal and external relationships of the Cnidaria: implications of primary and predicted secondary structure of the 5'-end of the 23S-like rDNA. Proc. R. Soc. Lond. B 264: 77-82.

Okubo, N., and T. Motokawa. 2007. Embryogenesis in the reef-building coral Acropora spp. Zool. Sci. 24: 1169-1177.

Ono, S., J. D. Reimer, and J. Tsukahara. 2005. Reproduction of Zoanthus sansibaricus in the infra-littoral zone at Taisho Lava Field, Sakurajima, Kagoshima, Japan. Zool. Sci. 22: 247-255.

Perse, J. S., J. B. McClintock, and I. Bosch. 1991. Reproduction of Antarctic benthic marine invertebrates: tempos, modes, and timing. Am. Zool. 31: 65-80.

Reimer, J. D., and C. Hickman. 2009. Preliminary survey of zooxan-thellate zoanthids (Cnidaria: Hexacorallia) of the Galapagos and associated symbiotic dinoflagellates (Symbiodinium spp.). Galapagos Res.66: 14-19.

Reimer, J. D., S. Ono, Y. Fujiwara, K. Takishita, and J. Tsukahara. 2004. Reconsidering Zoanthus spp. diversity: molecular evidence of conspecificity within four previously presumed species. Zool. Sci. 21: 517-525.

Reimer, J. D., S. Ono, K. Takishita, J. Tsukahara, and T. Maruyama. 2006. Molecular evidence suggesting species in the zoanthid genera Palythoa and Protopalythoa (Anthozoa: Hexacorallia) are congeneric. Zool. Sci. 23: 87-94.

Reimer, J. D., K. Takishita, S. Ono, and T. Maruyama. 2007a. Diversity and evolution in the zoanthid genus Palythoa (Cnidaria: Hexacorallia) utilizing nuclear ITS-rDNA. Coral Reefs 26: 399-410.

Reimer, J. D., K. Takishita, S. Ono, J. Tsukahara, and T. Maruyama. 2007b. Molecular evidence suggesting interspecific hybridization in Zoanthus spp. (Anthozoa: Hexacorallia). Zool. Sci. 24: 346-359.

Reimer, J. D., S. Nakachi, M. Hirose, E. Hirose, and S. Hashiguchi. 2010. Using hydrofluoric acid for morphological investigations of zoanthids (Cnidaria: Anthozoa): a critical assessment of methodology and necessity. Mar. Biotechnol. doi 10.1007/s 10126-009-9249-3.

Rentzsch, F., R. Anton, M. Saina, M. Hammerschmidt, T. W. Holstein, and U. Technau. 2006. Asymmetric expression of the bmp antagonists chordin and gremlin in the sea anemone Nematostella vectensis: implications for the evolution of axial patterning. Dev. Biol. 296: 375-387.

Richmond, R. H. 1997. Reproduction and recruitment in corals: critical links in the persistence of reefs. Pp. 175-197 in Life and Death of Coral Reefs, C. Birkeland, ed. Chapman and Hall, New York.

Ryland, J. S. 1997. Reproduction in Zoanthidea (Anthozoa, Hexacorallia). Invertebr. Reprod. Dev. 31: 177-188.

Ryland, J. S. 2000. Reproduction in British zoanthids and an unusual process in Parazoanthus anguicomus. J. Mar. Biol. Assoc. UK 80: 943-944

Ryland, J. S., and R. C. Babcock. 1991. Annual cycle of gametogen-esis and spawning in a tropical zoanthid, Protopalythoa sp. Hydrobio-logia 216/217: 117-123.

Ryland, J. S., and J. E. Lancaster. 2003. Revision of methods of separating species of Protopalythoa (Hexacorallia: Zoanthidea) in the tropical West Pacific. Invertebr. Syst. 17: 407-428.

Ryland, J. S., and A. Muirhead. 1993. Order Zoanthidea. Pp. 52-58 in A Coral Reef Handbook, P. Mather and I. Bennett, eds. Surrey Beatty, Chipping Norton, UK.

Ryland, J. S., S. de Putron., R. S. Scheltema., P. J. Chimonides., and D. G. Zhadan. 2000. Semper's (zoanthid) larvae: pelagic life, parentage and other problems. Hydrobiologia 440: 191-198.

Saina, M., G. Genikhovich., E. Renfer., and U. Technau. 2009. Bmps and chordin regulate patterning of the directive axis in a sea anemone. Proc. Natl. Acad. Sci. USA 106: 18592-18597.

Scheltema, R. S. 1971. The dispersal of larvae of shoal-water benthic invertebrate species over long distances by ocean currents. Pp. 7-28 in Fourth European Marine Biology Symposium, D. J. Crisp, ed. Cambridge University Press, Cambridge.

Semper, C. 1867. Ueber einige tropische Larvenfromen. Z. Wiss. Zool. 17: 407-428.

Shiroma, E., and J. D. Reimer. 2010. Investigations into the reproductive patterns, ecology, and morphology in the zoanthid genus Palythoa (Cnidaria: Anthozoa: Hexacorallia) in Okinawa, Japan. Zool. Stud. 49: 182-194.

Sinniger, F., and J. Pawlowski. 2009. The partial mitochondrial genome of Leiopathes glaberrima (Hexacorallia: Antipatharia) and the first report of the presence of an intron in COI in black corals. Galaxea 11: 21-26.

Sinniger, F., P. Chevaldonne., and J. Pawlowski. 2007. Mitochondrial genome of Savalia savaglia (Cnidaria, Hexacorallia) and early metazoan phylogeny. J. Mol. Evol. 64: 196-203.

van Beneden, E. 1897. Les Anthozoaires de la "Plankton-Expedition." Ergeb. Plankton-Exped. Humboldt Stift. II K: 485-521.

Veron, J. E. N., and C. C. Wallace. 1984. Scleractinia of Eastern Australia. Part 5. Family Acroporidae. Aust. Inst. Mar. Sci. Monogr. Ser. 6: 1-422.

Yamazato, K., F. Yoshimoto, and N. Yoshihara. 1973. Reproductive cycle in a zoanthid Palythoa tuberculosa Esper. Publ. Seto Mar. Biol. Lab. 20: 275-283.

MAMIKO HIROSE (1), (2), *, MASAMI OBUCHI (1), EUICHI HIROSE (2), AND JAMES D. REIMER (1), (3)

(1) Molecular Invertebrate Systematics and Ecology Laboratory, Rising Star Program, Transdisciplinary Research Organization for Subtropical Island Studies (TRO-SIS), University of the Ryukyus, Senbaru 1, Nishihara, Okinawa, 903-0213, Japan; (2) Faculty of Science, University of the Ryukyus, Senbaru 1, Nishihara, Okinawa, 903-0213, Japan; and (3) Marine Biodiversity Research Program, Institute of Biogeoscience, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Nastushima, Yokosuka, Kanagawa 237-0061, Japan

Received 29 July 2010; accepted 14 December 2010.

* To whom correspondence should be addressed. E-mail: mhirose@zenno.jp
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Author:Hirose, Mamiko; Obuchi, Masami; Hirose, Euichi; Reimer, James D.
Publication:The Biological Bulletin
Article Type:Report
Geographic Code:9JAPA
Date:Feb 1, 2011
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