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Comparative Embryology of Eleven Species of Stony Corals (Scleractinia)

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Comparative Embryology of Eleven Species of Stony Corals (Scleractinia) Comparative Embryology of Eleven Species of Stony Corals (Scleractinia) Nami Okubo1,5,7¤*, Takuma Mezaki2, Yoko Nozawa3, Yoshikatsu Nakano4, Yi-Ting Lien5, Hironobu Fukami6, David C. Hayward7, Eldon E. Ball7 1 Research and Education Center for Natural Sciences, Keio University, Yokohama, Kanagawa, Japan, 2 Kuroshio Biological Research Foundation, Hata, Kochi, Japan, 3 Biodiversity Research Center, Academia Sinica, Taipei, Taiwan, Republic of China, 4 Tropical Biosphere Research Center, Sesoko Station, Ryukyu University, Motobu, Okinawa, Japan, 5 Seto Marine Biological Laboratory, Field Science Education and Research Center, Kyoto University, Nishimuro, Wakayama, Japan, 6 Faculty of Agriculture, Miyazaki University, Gakuen-Kibanadai-Nishi, Miyazaki, Japan, 7 Evolution, Ecology and Genetics Group, Research School of Biology, Australian National University, Canberra, Australian Capital Territory, Australia Abstract A comprehensive understanding of coral reproduction and development is needed because corals are threatened in many ways by human activity. Major threats include the loss of their photosynthetic symbionts (Symbiodinium) caused by rising temperatures (bleaching), reduced ability to calcify caused by ocean acidification, increased storm severity associated with global climate change and an increase in predators caused by runoff from human agricultural activity. In spite of these threats, detailed descriptions of embryonic development are not available for many coral species. The current consensus is that there are two major groups of stony corals, the "complex" and the "robust". In this paper we describe the embryonic development of four "complex" species, Pseudosiderastrea tayamai, Galaxea fascicularis, Montipora hispida, and Pavona Decussata, and seven "robust" species, Oulastrea crispata, Platygyra contorta, Favites abdita, Echinophyllia aspera, Goniastrea favulus, Dipsastraea speciosa (previously Favia speciosa), and Phymastrea valenciennesi (previously Montastrea valenciennesi). Data from both histologically sectioned embryos and whole mounts are presented. One apparent difference between these two major groups is that before gastrulation the cells of the complex corals thus far described (mainly Acropora species) spread and flatten to produce the so-called prawn chip, which lacks a blastocoel. Our present broad survey of robust and complex corals reveals that prawn chip formation is not a synapomorphy of complex corals, as Pavona Decussata does not form a prawn chip and has a well-developed blastocoel. Although prawn chip formation cannot be used to separate the two clades, none of the robust corals which we surveyed has such a stage. Many robust coral embryos pass through two periods of invagination, separated by a return to a spherical shape. However, only the second of these periods is associated with endoderm formation. We have therefore termed the first invagination a pseudo-blastopore. Citation: Okubo N, Mezaki T, Nozawa Y, Nakano Y, Lien Y-T, et al. (2013) Comparative Embryology of Eleven Species of Stony Corals (Scleractinia). PLoS ONE 8(12): e84115. doi:10.1371/journal.pone.0084115 Editor: Mónica Medina, Pennsylvania State University, United States of America Received June 6, 2013; Accepted November 12, 2013; Published December 18, 2013 Copyright: © 2013 Okubo et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: NO was supported for this study by a Grant-in-Aid for JSPS Fellows (Grant No. 222948) and a Grant-in-Aid for Young Scientists (B) (Grant No. 13221488) from the Japan Society for the Promotion of Science (http://www.jsps.go.jp). Further support was received from Tokyo Keizai University (Research Grant 12-01). EEB and DCH were supported by the Australian Research Council (http://www.arc.gov.au/) through Discovery Grant (#DP1095343). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. * Email: [email protected] ¤ Current address: Department of Economics, Tokyo Keizai University, Kokubunji, Tokyo, Japan Introduction planulae are released. Considerably less is known about their patterns of early development, the topic of this paper. Corals are highly variable in their reproductive patterns. Based on molecular sequence data, scleractinian corals can There are species in which colonies may have a single sex be divided into two large clades, the robust and the complex, throughout life, while other species may be sequential that appear to have diverged more than 200MYA [1-5]. For hermaphrodites, with sex based on size, or simultaneous many years, before the widespread availability of sequence hermaphrodites. They may also be synchronous spawners, data, coral taxonomy was based on morphological characters releasing eggs and sperm or egg-sperm bundles, or brooders (e.g. 6,7) but few of the families created on this basis are in which early development takes place within the colony and presently regarded as monophyletic based on recent molecular PLOS ONE | www.plosone.org 1 December 2013 | Volume 8 | Issue 12 | e84115 Comparative Embryology of Coral studies [8]. Indeed, 8 of the 24 extant families recognized by abdita, Echinophyllia aspera, Goniastrea favulus, Pavona Fukami et al. [2] have representatives in both the robust and Decussata and Phymastrea valenciennesi (previously complex clades [4]. Thus, the details of coral phylogeny are Montastrea valenciennesi) in Kochi Prefecture; embryos of presently the subject of much debate, as is reflected in the title Dipsastraea speciosa (previously Favia speciosa) and of a recent paper on the phylogeny of four coral families, which Oulastrea crispata in Wakayama Prefecture. We hope that this begins "Cleaning up the 'Bigmessidae' " [9]. Nevertheless, paper will help to make people aware of the importance of coral there appears to be general agreement on the existence of the embryos in coral conservation. two large clades mentioned above; the robust (so called because they are plate-like or massive) and complex (so called Embryo collection because they have diverse growth forms and are less heavily Gametes of Galaxea fascicularis were collected from Sesoko calcified), which were first proposed by Romano and Palumbi Marine Biological Laboratory in Okinawa (26°63′ N, 127°86′ E); [1] on the basis of mitochondrial 16S ribosomal gene Pseudosiderastrea tayamai from Ogimi-son, Okinawa, Japan sequences. Figure S1 shows the species studied here mapped (26°70′ N, 128°12′ E); Montipora digitata and Montipora hispida onto the phylogeny of Kitahara et al [3] and demonstrates that from the reefs around Akajima Island, Okinawa (26°27′ N, they are well distributed across the two major groups. 127°28′ E); Favites abdita, Favites pentagona, Goniastrea Because most corals spawn at night, and in some cases only favulus, Phymastrea valenciennesi and Pavona Decussata once per year, descriptions of the development of many from near the Laboratory of Kuroshio Biosphere Foundation, species are still fragmentary. This is in spite of the increasingly Kochi (32°78′ N, 132°73′ E); and Dipsastraea speciosa, widespread interest in the group, which has developed as the Echinophyllia aspera, Oulastrea crispata and Platygyra threats posed by human activity have become recognized. This contorta from Tanabe Bay near Kyoto Field Science Center, lack of knowledge is particularly acute for the earliest stages of Wakayama (33°69′ N, 135°33′ E). The dates of all of these development up to and including gastrulation, which are collections are given in Table 1 along with additional locality, passed through quite rapidly. habitat and spawning data. In some species, colonies were Although there have been several reviews of coral reproduction and development in recent decades (e.g. 8,10-12) brought to the laboratory where spawning occurred in tubs. these have not dealt with the details of early development, Once spawning had occurred, gametes were gently stirred to which are found only in the primary literature, where the mix the bundles and ensure insemination. For these species coverage is extremely patchy, with considerable detail the number of colonies involved in the crosses is given in available for some species and none for others. We here brackets. In other species gametes were collected by divers on describe the early development of four complex corals; SCUBA from the surface of colonies as they spawned. These Pseudosiderastrea tayamai, Galaxea fascicularis, Montipora species are marked with an asterisk and in all cases 3 or more hispida and Pavona Decussata and seven robust corals; colonies were sampled. For all species, fertilized eggs were Oulastrea crispata, Platygyra contorta, Favites abdita, placed into 2.5L containers in filtered sea water and Echinophyllia aspera, Goniastrea favulus, Dipsastraea development allowed to proceed. Gametes and the early speciosa (previously Favia speciosa), Phymastrea stages of development were sampled and examined hourly for valenciennesi (previously Montastrea valenciennesi: the last the first 24 h after spawning and every 4 or 6 h thereafter. two genera were renamed in a recent taxonomic revision by Typically, each container held more than 1000 embryos and at Budd et al. [13]). As far as we are aware, development
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