Microscopic observations of larval Ostrea circumpicta (bivalve: ostreidae) in brood chambers.ABSTRACT This study is the first report of the microscopic features of larvae and gonads of Ostrea circumpicta collected in Jeju, Korea. Female oysters brooded larvae at the early veliger ve·li·ger n. A larval stage of a mollusk characterized by the presence of a velum. [New Latin v stage (115-135 [micro]m) in the infrabranchial chamber. Larvae in this chamber displayed a well-developed velum velum /ve·lum/ (ve´lum) pl. ve´la [L.] a covering structure or veil.ve´lar velum interpo´situm ce´rebri membranous roof of the third ventricle. covered with long and short cilia cilia /cil·ia/ (sil´e-ah) sing. cil´ium [L.] 1. the eyelids or their outer edges. 2. the eyelashes. 3. : the adductor muscle Noun 1. adductor muscle - a muscle that draws a body part toward the median line adductor skeletal muscle, striated muscle - a muscle that is connected at either or both ends to a bone and so move parts of the skeleton; a muscle that is characterized by was incompletely developed. The digestive system of the larvae, including the mouth, esophagus, stomach, digestive gland, and intestine, was identifiable in histologic preparations, indicating that the veliger larvae in the brood chamber were capable of feeding using the velum and cilia. Diameters of ripe eggs in the ovary ranged from 67-120 [micro]m. Most female oysters collected in June 2001 were spawning or absorbing whereas most of male oysters were spent or sexually inactive. KEY WORDS: ostreidae, Ostrea circumpicta, reproduction, larval morphology, brood oyster, Korea INTRODUCTION Oysters of the genus Ostrea are brooders, releasing larvae instead of gametes during spawning (Buroker 1985, O Foighil & Taylor 2000). Gametes of brood oysters are fertilized at the ctenidia, and the embryos are released into the branchial branchial /bran·chi·al/ (brang´ke-al) pertaining to or resembling gills of a fish or derivatives of homologous parts in higher forms. bran·chi·al adj. chamber of females. In this chamber, the larvae undergo pelagic pelagic living in the middle or near the surface of large bodies of water such as lakes or oceans. development, including trochopore and veliger stages (Strathmann & Strathmann 1982, Mackie 1984, O Foighil & Taylor 2000). Veliger larvae in the chamber are characterized by velum covered with cilia that are used for locomotion and feeding (Elston 1999, Chaparro et al. 1999 & 2002). Swimming veliger larvae are often observed in suprabrachial or infrabranchial chambers (Chaparro et al. 1993). However, brooding oyster larvae are often kept in interlamellar spaces or brood sacs and are immobile (Mackie 1984, Tankersley & Dimock 1992). Microscopic examination of larvae provides valuable information on feeding type, developmental mode, planktonic period, and larval settlement (Strathmann & Leise 1979, Pechenik 1986, Strathmann et al. 1993, Chaparro et al. 1999). Histology has been widely and extensively used to examine the larval structure and development of marine bivalves (Howard & Smith 1983, Elston 1999). In addition, video cameras and endoscopes are often used in microscopic observations of marine bivalve bivalve, aquatic mollusk of the class Pelecypoda ("hatchet-foot") or Bivalvia, with a laterally compressed body and a shell consisting of two valves, or movable pieces, hinged by an elastic ligament. larvae (Ward et al. 1991, Strathmann et al. 1993, Tankersley & Dimock 1993, Bosch & Slattery 1999, Elston 1980, Chaparro et al. 1999&2002). Ostrea circumpicta is abundant on rocky intertidal in·ter·tid·al adj. Of or being the region between the high tide mark and the low tide mark. in to subtidal zones of Jeju Island (Kwon et al. 1993), Korea, where salinity remains high and stable all year (Lee et al. 2000). Like other oysters of the genus Ostrea, this species is a brooder brooder stage two of the usual bird rearing sequence. After hatching the baby birds are put into a brooder house, usually with a heat source attached, for rearing. Also used as a management strategy for baby pigs which are weaned early, at 3 weeks. and is widely distributed in southern Japan, China, and Korea (Hirase 1930, Bernard et al. 1993, Kwon et al. 1993). Despite its abundance, few studies have investigated the ecology and reproductive biology of O. circumpicta (Bae & Bae 1972, Yang 1999&2001). Here, we provide the first report of the microscopic features of the gonads and larvae of O. circumpicta in sexually mature individuals. MATERIALS AND METHODS Munseom, an uninhabited island located off the southern coast of Jeju (33 [degrees]13' 25"N, 126 [degrees]33' 58"E), is well known for its high species diversity and richness of marine biota biota /bi·o·ta/ (bi-o´tah) all the living organisms of a particular area; the combined flora and fauna of a region. bi·o·ta n. The flora and fauna of a region. (Je et al. 2002, Fig. 1). The island characterized by volcanic rocky intertidal and subtidal zones that are subjected to strong wave action. The rocky substrata are enriched with sessile sessile /ses·sile/ (ses´il) attached by a broad base, as opposed to being pedunculated or stalked. ses·sile adj. Permanently attached or fixed; not free-moving. fauna such as oysters, barnacles, and numerous species of anthozoans. In particular. O. circumpicta heavily encrusts the subtidal cliff at depths between 3 and 6 m. Surface water temperatures and salinity in this area vary from 16 [degrees]C to 22 [degrees]C and from 32.2 34.4 psu annually (Choa & Lee 2000, Lee et al. 2000). Due to the influence of the warm Kuroshio current, surface water temperatures during winter are several degrees higher than in northern Jeju. [FIGURE 1 OMITTED] O. circumpicta were collected in June 2003 by SCUBA diving at depths between 3 and 5 m. Oyster tissues were fixed in Davison's fixative fixative /fix·a·tive/ (fik´sit-iv) an agent used in preserving a histological or pathological specimen so as to maintain the normal structure of its constituent elements. fix·a·tive adj. , and longitudinal sections were made along the middle of the body of fixed specimens (Fig. 2A) using standard histologic methods. Microscopic images of oyster eggs and larvae in brood chambers were converted to digital image using a digital camera installed on the microscope. The size of eggs and larvae were then measured from the images using image analysis software (Kang et al. 2003). [FIGURE 2 OMITTED] RESULTS Figure 2 shows a female O. circumpicta collected in June 2003. This species has a relatively large adductor muscle and gills compared with nonbrooding oysters. The mantle is composed of two layers with thick mantle lobes. We found no hermaphroditic her·maph·ro·dite n. 1. An animal or plant exhibiting hermaphroditism. 2. Something that is a combination of disparate or contradictory elements. individuals in this study. Figure 3 shows numerous early veliger larvae in the infrabranchial chamber. The visceral masses of the larvae were filled with coelomic fluid in the coelomic cavity. The larvae were approximately 115-135 [micro]m long, and we observed no physical connections between female oysters and larvae. No obvious structural changes for holding larvae were found in the gills. Figure 4 shows intact larvae isolated from the chamber. The upper part of the velum was covered with two types of cilia; long outer preoral pre·o·ral adj. Situated or located in front of the mouth. preoral situated rostral to the mouth; in front of the mouth. cilia (i.e., OPC (1) (OpenGL Performance Characterization) A project group within GPC that manages OpenGL benchmarks. OPC endorses the Viewperf and GLperf benchmarks. Viewperf was created by IBM and OPC provides viewsets for it, which are combinations of tests using specific , Chaparro et al. 1999), 20-40 [micro]m long and short inner preoral cilia (IPC (1) (InterProcess Communication) The exchange of data between one program and another either within the same computer or over a network. It implies a protocol that guarantees a response to a request. ), 5-10 [micro]m long. [FIGURES 3-4 OMITTED] Figures 5 and 6 illustrate the internal structure of early veliger larvae. The mouth is located at the edge of the lower part of the velum, and the oral opening lead to the esophagus. The stomach is visible at the end of the digestive tract. The larval stomach, digestive gland, and intestine form the digestive system. Although it is not completely developed, the adductor muscle is identifiable in the larvae. Cilia are mainly located on the periphery of the velum: sensory cilia are also found on the apical apical /ap·i·cal/ (ap´i-k'l) pertaining to an apex. a·pi·cal adj. 1. Relating to the apex of a pyramidal or pointed structure. 2. plate located at the center of the velum. Some particles were identified in the digestive gland that were believed to be ingested diatoms diatoms a series of unicellular algae, microscopic in size, with cell walls containing silica. Members of the family Diatomaceae. Their remains accumulate as geological deposits and are mined. See diatomaceous earth. (Kohn, personal communication). [FIGURES 5-6 OMITTED] Figure 7 shows a longitudinal section of female oyster whose follicles follicles, n the masses that are embedded in a meshwork of reticular fibers within the lobules of the thyroid gland. See also thyroid gland. are packed with ripe eggs (see Fig. 7A). The diameter of egg nuclei ranged from 16-35 [micro]m, with a mean of 26 [micro]m (n = 29). Egg diameter ranged from 67-120 [micro]m, with a mean of 89 [micro]m (n = 60). However, most ripe eggs were ready for discharging from the follicles 9-110 [micro]m in diameter. Some degenerating ova ova (o´vah) plural of ovum. Ova Eggs. Mentioned in: Stool O & P Test ova plural of ovum. were surrounded by hemocytes, indicating that the eggs are phagocytosed by hemocytes (see Fig. 7B). Nine male oysters analyzed in this study exhibited spent testes or were in sexually inactive (see Figs. 7C, 7D), indicating that males spawned earlier than females. [FIGURE 7 OMITTED] DISCUSSION In marine bivalves, fertilization and development of larvae is either external or internal (Sastry 1979, Strathmann & Strathmann 1982, Olive 1985, Levitan & Petersen 1995). Oysters of the genus Crassostrea broadcast eggs and sperm in the water column, and fertilization and subsequent larval development occurs externally. In contrast, in oysters of the genus Ostrea, egg fertilization takes place internally in the gills (Andrews 1979, Harry 1985, Chaparro et al. 1993, O Foighil & Taylor 2000). The embryos or larvae are then raised in the mantle cavity, suprabranchial, or infrabranchial chamber of the female (Buroker 1985, Chaparro et al. 1993, O Foighil & Taylor 2000). In this study, larvae were located mostly in the infrabranchial chamber (see Figs. 2, 3), indicating that O. circumpicta uses its gills as a brooding chamber, as has been observed in other brooding oysters of the genus Ostrea. Early veliger larvae located in the infrabranchial chamber showed a well developed velum covered with cilia (see Figs. 5, 6). The presence of a cilial ring around the velum is one of the key characteristics of veliger larvae (Waller 1981, Beauchamp 1986, Strathmann et al. 1993, Chaparro et al. 1999). Cragg (1989) suggested that a well developed velum with cilia is an adaptation for prolonged planktonic life in the water column. The velum also plays a key role in feeding during the larval period (Hadfield et al. 1997, Klinzing & Pechenik 2000, Chaparro et al. 2002). Larvae in the brood chamber observed in this study exhibited a well-developed digestive system that included the mouth, esophagus, stomach, digestive gland, and intestine (see Fig. 5). Longitudinal section of the larvae also showed some food-like particles in the digestive gland (see Fig. 5), suggesting that the larvae are involved in feeding activities (Elston, 1999). Chaparro et al. (1993) experimentally fed the veliger larvae of O. chiliensis with plastic particles (2-10 [micro]m in diameter), and the particles were later found in the digestive system. Their study indicated that the veligers were actively involved in feeding activities in the brood chamber. Thus, it is believed that O, circumpicta veliger larvae also feed on food particles available in the brood chamber, as was observed in O. chiliensis. The size of the O. circumpicta egg measured in this study varied from 67-120 [micro]m, which is somewhat larger than the eggs of nonbrooding oysters such as C. gigas or C. virginica (40-58 [micro]m, Gallager et al. 1986, Arakawa 1990, Choi et al. 1993, Brousseau 1995, Lango-Reynoso et al. 2000, Kang et al. 20(13). The relatively larger egg size of O. circumpicta suggests that these oysters produce lecithotrophic eggs, like O. edulis, O. denselamellosa, or O. lurida (DiSalvo et al. 1983, Mackie 1984, Arakawa 1990). DiSalvo et al. (1983) reported that O. chilensis larvae in Chilean waters do not ingest food particles when reared outside the brooding chamber, strongly indicating that O. chilensis larvae are truly lecithotropic. In contrast, Chaparro et al. (1993; 1999) used an endoscope to observe veligers of O. chilensis (290-300 [micro]m) actively feeding on food particles available in the brood chamber that experimentally provided. The authors concluded that O. chilensis larvae are planktotrophic, because they have a complete digestive system and feed on food particles in the chamber, The O. circumpicta larvae observed in this study were 115-135 [micro]m long (i.e., slightly larger than mature eggs 190-110 [micro]m]), indicating that the larvae were in the early veliger stage. Food-like particles found in the digestive system of O. circumpicta veliger larvae in this study suggest that the larvae are planktotrophic in the brood chamber. In conclusion, we observed the larval development of O. circumpicta in the infrabranchial chamber using histologic preparations. Ripe and degenerating ova in the gonads and early veliger larvae in brood chamber observed in late June indicated that late June, when water temperature reaches 22 [degrees]C, is the spawning. A well-developed velum and digestive system suggested that the larvae are capable of swimming and feeding inside the brood chamber. ACKNOWLEDGMENTS The authors thank the staff of shellfish research and aquaculture aquaculture, the raising and harvesting of fresh- and saltwater plants and animals. The most economically important form of aquaculture is fish farming, an industry that accounts for an ever increasing share of world fisheries production. laboratory of Cheju National University Cheju National University is the smallest one among 10 major national universities in Korea along with Seoul National University, Pusan National University Kyungpook National University, Chonnam National University, Chungnam National University, Chonbuk National University, . The authors also thank to Dr. Alan J. Kohn for comments and critique of the manuscript. This work was supported by a grant (No. BDM BDM Black Divorced Male BDM Business Development Manager BDM Background Debug(ger) Mode BDM Bund Deutscher Mädel (League of German Girls during the Third Reich, akin to Hitler Youth) 0100211) to JRL JRL - J. Random Loser. The names JRL and JRN were sometimes used as example names when discussing a kind of user ID used under TOPS-10 and WAITS. They were understood to be the initials of (fictitious) programmers named "J. Random Loser" and "J. Random Nerd". from the Strategic National R&D Program through the Genetic Resources and Informatica Network Center funded by the Ministry of Science and Technology, Korea. LITERATURE CITED Andrews, J. 1979. Pelecypoda: Ostreidae. In: A. Giese & J. Pearse, editors. Reproduction of marina invertebrates. New York: Academic Press Inc. pp. 293-341. Arakawa, K. 1990. 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