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Reproduction in Anthelia Glauca (Octocorallia: Xeniidae). II

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Reproduction in Anthelia Glauca (Octocorallia: Xeniidae). II Marine Biology (1998) 131: 433±442 Ó Springer-Verlag 1998 Y. Benayahu á M. H. Schleyer Reproduction in Anthelia glauca (Octocorallia: Xeniidae). II. Transmission of algal symbionts during planular brooding Received: 15 July 1997 / Accepted: 25 February 1998 Abstract The soft coral Anthelia glauca Lamarck, 1816, major faunistic component in many areas (e.g. Roxas of the family Xeniidae, is found on the reefs of KwaZulu- 1933; Gohar 1940; Benayahu 1985, 1990). Life-history Natal, South Africa. Its gastrodermal cells contain nu- features and various ecological aspects of several xeniid merous endosymbiotic unicellular algae (zooxanthellae). species have been extensively examined (e.g. Gohar A. glauca is a gonochoric species that simultaneously 1940; Benayahu and Loya 1984a, b; Dinesen 1985; Alino broods its planulae within the pharyngeal cavity of the and Coll 1989; Benayahu 1991). To date, all members of polyps. Symbiotic algae appear with zygote formation this family are known to brood planulae (Gohar 1940; within the pharynx, embedded in amorphous material. Benayahu 1991, 1997). However, both the mode and the The algal cells adhere to the ciliated ectodermal surface site of brooding vary among genera. In Xenia species, of immature planulae and are most probably endo- the planulae develop inside brooding pouches located cytosed by them. Zooxanthellae are translocated towards below the anthocodia among the polyp cavities (Bena- the basal part of the ectoderm. Gaps are subsequently yahu and Loya 1984b; Benayahu et al. 1988; Achituv opened in the mesoglea into which symbionts sur- et al. 1992). Heteroxenia species are elaborate in their rounded by ectodermally derived material, including brood care, with early embryogenesis occurring inside plasma membrane, pass. The basal membrane of endo- the gastrovascular cavities of either the anthocodia or dermal cells disintegrates, and the algae bulge into spaces the tentacles, and subsequent development and matu- formed in the underlying endoderm. Throughout the ration of planulae taking place in the intersiphonozooid process, each zooxanthella resides within a vacuolar spaces (Benayahu 1991). Eatounaria sp. is an external- membrane in the detached ectodermal cytoplasm. The surface brooder (Dinesen 1985; Alino and Coll 1989). In acquisition process is essentially one in which zooxa- Sympodium caeruleum, planulae have been found within nthellae are translocated fromthe pharyngeal cavity into the gastrovascular cavities (Benayahu 1991). To date, no the ectodermand then through the mesoglea into the information is available on the reproduction of the other endoderm, culminating in the ®nal symbiotic state. The xeniid genera, Cespitularia and Fungulus. An early study direct transmission of symbiotic algae to the eggs or by Gohar (1940) noted that the xeniid Anthelia glauca larvae probably provides the most ecient means reproduces by planular release. This ®nding has recently whereby zooxanthellae are acquired by the host progeny. been con®rmed, and, in addition, a unique brooding mode within the pharyngeal cavity of the polyps has been described for this species (Kruger 1996; Schleyer Introduction et al. 1997; Kruger et al. 1998). Numerous reef cnidarians, including all known xeniid Octocorals of the family Xeniidae are common soft corals, harbor numerous endosymbiotic algae throughout the Indo-Paci®c reef systemand constitute a (zooxanthellae) in their gastrodermal tissue (Gohar 1940; Schlichter 1982; Benayahu et al. 1988). Utilization of the products of algal photosynthesis and even the Communicated by O. Kinne, Oldendorf/Luhe symbionts themselves is of major nutritional importance for Heteroxenia fuscescens of the family Xeniidae Y. Benayahu (&) Department of Zoology, George S. Wise Faculty of Life Sciences, (Schlichter 1982). Several studies have addressed the Tel Aviv University, Ramat Aviv, Tel Aviv 69978, Israel question of the developmental stage at which the sexu- ally produced ospring of symbiotic hosts acquire their M.H. Schleyer Oceanographic Research Institute, P.O. Box 10712, algal symbionts (e.g. Muscatine 1974; Fitt 1984; Trench Marine Parade 4056, Durban, Republic of South Africa 1987). Trench (1987) proposed two modes of acquisition 434 of the symbiotic algae: either by direct transmission via verrucosa on the South African reefs, conducted fromSeptember the egg or brooded larvae (maternal inheritance), or 1991 to September 1994 (Kruger 1996; Schleyer et al. 1997). The population of Anthelia glauca was sampled every 1 to from the ambient environment (open system), by post- 2 months throughout the years 1992 to 1994 in order to study the larval stages. Direct transmission of symbionts has been gonadal cycle and ascertain the reproductive season (Kruger et al. documented in species of the cnidarian classes Hydrozoa 1998). In 1993 and 1994, sampling of colonies was intensi®ed (e.g. Trench 1987; Campbell 1990), Scyphozoa (Mont- during the months January to March, the peak breeding season gomery and Kremer 1995) and Anthozoa (e.g. Glynn (Kruger 1996; Schleyer et al. 1997). On each sampling date eight to ten specimens were removed from Nine-mile Reef (27°24.9¢S; et al. 1991; Benayahu et al. 1992; Benayahu 1997). Ac- 32°43.6¢E) in the central reef complex of Sodwana Bay by SCUBA quisition of symbionts from the ambient environment is divers. Material for light microscopy was ®xed for 24 h in 4% far more common than maternal inheritance, and occurs formaldehyde in seawater, rinsed carefully in fresh water and then both in scleractinian corals (Babcock et al. 1986; Har- transferred into 70% ethanol. These samples were decalci®ed in formal-nitric acid solution (Mahoney 1966) and passed through rison and Wallace 1990; Shlesinger and Loya 1991) and methanol, ethanol and isopropanol in a Biorad tissue processor octocorals (Kinzie 1974; Benayahu et al. 1989). Eggs before embedding in paraplast. Sections, 5 lmthick, were cut on a broadcast by the vast majority of species of both these microtome and stained with Ehrlich's haemalum and eosin (Drury groups lack algal symbionts upon release, as opposed to and Wallington 1967). The material for transmission electron mi- croscopy (TEM) was ®xed in 4% glutaraldehyde in sea water and brooders which release mostly zooxanthellate larvae decalci®ed in a mixture of equal volumes of formic acid (50%) and (Babcock et al. 1986; Harrison and Wallace 1990). sodiumcitrate (15%) for 30 min.It was dehydrated in a graded Among the Xeniidae, Xenia species release zooxanthel- series of ethyl alcohol and embedded in Epon. Sections stained in late planulae, whose symbionts are incorporated at an uranyl acetate and lead citrate were viewed with a Jeol 1200EX early embryonic stage (Benayahu and Loya 1984b; electron microscope. Benayahu et al. 1988). Heteroxenia species release azooxanthellate planulae, and algal uptake occurs at an early primary polyp stage (Benayahu et al. 1989). Results Species of the xeniid genus Anthelia are less abundant on Indo-Paci®c reefs than those of Xenia or Heteroxenia The brood of Anthelia glauca is found within the pha- (Benayahu 1985; personal observations). A. glauca has ryngeal cavity (Schleyer et al. 1997; Kruger et al. 1998), been recorded on many Indo-Paci®c reefs and seems to and it thus neighbors an epidermal milieu (Fig. 1a, b). be the most abundant species of its genus (e.g. Roxas The underlying thin mesoglea delimits the gastrodermis 1933; Gohar 1940; Benayahu 1990, 1993). This soft coral that lines the gastrovascular cavity (Fig. 1a±c). Only the is gonochoric, bears gonads throughout the year and gastrodermal cells of the colonies harbor the symbiotic reproduces by releasing planulae over a period of 3 to zooxanthellae in A. glauca (Fig. 1b). The mesenteries of 4 months a year (Kruger et al. 1998). The current study the polyp are attached to the pharyngeal wall, and their focuses on the mode of transmission of algal symbionts mesoglea and gastrodermis are continuous with the re- to brooded planulae of A. glauca. We describe the spective layers of both the pharynx and polyp wall stepwise process of algal infection and movement into (Fig. 1a, c). The earliest developmental stage observed in endodermal cells. Uptake of zooxanthellae is appar- the pharyngeal cavity consisted of zygotes (Fig. 1a, b), ently initiated at an immature planula stage, where which lacked both a follicular cell layer and underlying symbionts are translocated from seawater in the pha- mesoglea found around the oocytes (see also Benayahu ryngeal cavity into the planular ectoderm. Symbionts 1997). Patches of amorphous material were found are subsequently detached, surrounded by ectodermally among the zygotes (Fig. 1a, b), in which symbiotic algae derived plasma membrane and some cellular debri, and eventually become embedded (Fig. 1c, d). At this stage, translocated through the mesoglea into the endodermal layer. The implications of these features are discussed c in relation to previously described modes of symbiont Fig. 1 Anthelia glauca. All histological sections. a Zygotes adjacent to acquisition, and their developmental consequences are the ectodermal lining (arrows) within pharyngeal cavity ( ph)and considered. surrounded by amorphous material (asterisk). The gastrovascular cavity (gv) is lined by gastrodermis (gs) and divided by septa attached to the pharyngeal wall, both with a continuous mesoglea (m). Scale: 120 lm. b Zygote surrounded by amorphous material (asterisk) Materials and methods within pharyngeal cavity (ph) adjacent to the darkly
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