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Sexual Reproduction in Octocorals

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Sexual Reproduction in Octocorals Vol. 443: 265–283, 2011 MARINE ECOLOGY PROGRESS SERIES Published December 20 doi: 10.3354/meps09414 Mar Ecol Prog Ser REVIEW Sexual reproduction in octocorals Samuel E. Kahng1,*, Yehuda Benayahu2, Howard R. Lasker3 1Hawaii Pacific University, College of Natural Science, Waimanalo, Hawaii 96795, USA 2Department of Zoology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Ramat Aviv, Tel Aviv 69978, Israel 3Department of Geology and Graduate Program in Evolution, Ecology and Behavior, University at Buffalo, Buffalo, New York 14260, USA ABSTRACT: For octocorals, sexual reproductive processes are fundamental to maintaining popu- lations and influencing macroevolutionary processes. While ecological data on octocorals have lagged behind their scleractinian counterparts, the proliferation of reproductive studies in recent years now enables comparisons between these important anthozoan taxa. Here we review the systematic and biogeographic patterns of reproductive biology within Octocorallia from 182 spe- cies across 25 families and 79 genera. As in scleractinians, sexuality in octocorals appears to be highly conserved. However, gonochorism (89%) in octocorals predominates, and hermaphro- ditism is relatively rare, in stark contrast to scleractinians. Mode of reproduction is relatively plas- tic and evenly split between broadcast spawning (49%) and the 2 forms of brooding (internal 40% and external 11%). External surface brooding which appears to be absent in scleractinians may represent an intermediate strategy to broadcast spawning and internal brooding and may be enabled by chemical defenses. Octocorals tend to have large oocytes, but size bears no statistically significant relationship to sexuality, mode of reproduction, or polyp fecundity. Oocyte size is sig- nificantly associated with subclade suggesting evolutionary conservatism, and zooxanthellate species have significantly larger oocytes than azooxanthellate species. Based on biogeographic patterns, reef scleractinians appear to disperse longer distances over ecological timescales com- pared to reef octocorals. However, differences in reproductive characteristics between the 2 taxa do not offer an obvious explanation for these different biogeographic patterns. KEY WORDS: Octocoral · Sexual reproduction · Coral reef · Life history · Biogeography Resale or republication not permitted without written consent of the publisher INTRODUCTION of 2 clades with a few taxa belonging to a much smaller third clade. Approximately 274 of the Octocorals are a diverse and widespread group genera belong to the most speciose order, Alcy- of marine organisms ranging across all latitudes onacea, and some genera are very speciose includ- and across depths from the intertidal zone to ing the Indo-Pacific coral reef genus Sinularia abyssal plains (Bayer 1981). The class Octocorallia which has over 150 species (McFadden et al. 2009). has ~310 genera distributed among 3 orders: Helio- Species of Alcyonacea include forms commonly poracea, Alcyonacea, and Pennatulacea (Bayer known as soft corals, sea fans, and sea whips, and 1981). However, based on molecular data, McFad- this order generally corresponds to the Alcyoniina/ den et al. (2006) suggested that the orders are poly- Holoxonia clade hypothesized by McFadden et al. phyletic and that most octocoral taxa are members (2006). *Email: [email protected] © Inter-Research 2011 · www.int-res.com 266 Mar Ecol Prog Ser 443: 265–283, 2011 In many coral reef ecosystems, particularly in the ductive patterns of stony corals (Scleractinia) have Caribbean and some Indo-West Pacific reefs, shallow- been the center of intense study in recent decades water octocorals are a major, sometimes dominant, (Fadlallah 1983, Szmant 1986, Harrison & Wallace faunistic component (Bayer 1981, Benayahu & Loya 1990, Richmond & Hunter 1990, Richmond 1997, 1981, Dinesen 1983, Sammarco & Coll 1992, Spalding Shlesinger et al. 1998, Baird et al. 2009, Harrison et al. 2001). Among reef octocorals, the majority of 2011). Given the abundance of both scleractinians species are zooxanthellate, possessing endosymbiotic and octocorals in tropical reef ecosystems and the microalgae in their tissues. However, many Indo- ecological similarities between them, a thorough Pacific and some Caribbean reef species are azooxan- compilation of the available octocoral data and com- thellate (Fabricius & Alderslade 2001). In deep-water parison of their reproductive strategies with those of ecosystems, octocorals are important structure-form- scleractinians can indicate whether reproductive ing organisms that colonize substrata in dense aggre- strategies in the 2 groups have paralleled each other. gations and create critical habitat for associated fauna (Lumsden et al. 2007, Messing et al. 2008). Like many species of Anthozoa, octocorals are METHODS almost exclusively modular colonial marine inverte- brates that reproduce both sexually and asexually. The octocoral reproductive traits considered in the As in all modular organisms, colony growth is a mode analyses are listed in Table 1. Data were gathered of asexual reproduction via budding of polyps. In through an exhaustive search of the literature, com- addition, octocorals exhibit a diversity of mechanisms munication with other researchers, and our own of vegetative propagation including simple fission, unpublished data. However, as apparent from Table fission by partial mortality, fragmentation, polyp S1 (see electronic supplement, available at www.int- detachment, budding, branching growth, and sto - res.com/articles/suppl/m443p265_supp.pdf, obtaining lonal growth (Lasker 1988). For some species, asex- complete information for many of the species was not ual, vegetative propagation can support high popula- possible. However, basic information such as sexual- tion growth rates (Lasker 1988). All octocorals that ity and the modes of larval development were avail- have been studied in detail reproduce sexually. The able for the vast majority of species. dual modes of reproduction allow species to follow multiple ecological strategies (Jackson 1985). How- ever, sexual reproduction remains the dominant Systematics mode of population growth for most species. Sexual reproduction and the dispersal of the resultant larval Among octocorals, morphological characters have stage control the connectivity of populations and been traditionally used to distinguish between taxa. maintains the genetic diversity in octocorals as in all These particularly include colony growth form, axial benthic invertebrates (Jackson 1986). structure, and the size, shape, micro-architecture, and Until the early 1970s, most of the knowledge on arrangement of sclerites (e.g. Bayer 1961, Berntson et the reproduction of octocorals had been based on al. 2001, Alderslade 2001, Fabricius & Alderslade studies of a small number of species. Some of the 2001). Attempts to understand their phylogenetic re- earliest studies characterized reproduction in the lationships have been hampered by a paucity of widespread boreal species Alcyonium digitatum useful morphological characters and consequently led (e.g. de Lacaze-Duthiers 1864, Hickson 1895, 1901, to molecular phylogenetic analysis of this group. Mc- Hill & Oxon 1905, Matthews 1917). The pioneering Fadden et al. (2006) presented mitochondrial DNA study of Kowa lewsky & Marion (1883) examined the (mtDNA) analyses that convincingly argued that most embryogenesis of Clavularia crassa, C. petricola of the currently recognized families and suborders in and Sympodium coralloides and depicted detailed the Octocorallia are polyphyletic. However, a revision images of planula-development. Gohar (1940a,b) of the higher taxa has not yet been made. In our treat- and Gohar & Roushdy (1961) provided valuable ment we continue to refer to the traditionally recog- information on reproduction of the Red Sea soft nized families since most readers are familiar with corals from the family Xeniidae. them (see also Fabricius & Alderslade 2001). Although A growing number of reproductive studies of octo- there are some important inconsistencies, they do corals have been undertaken in recent years, but the have a general congruence to the patterns reported in reproductive patterns of octocorals have never been McFadden et al. (2006). However, in our statistical comprehensively reviewed. In contrast, the repro- analyses we use Clades 1, 2 and 3 as recognized by Kahng et al.: Sexual reproduction in octocorals 267 Table 1. Reproductive traits and other factors considered for each octocoral species in this study Characteristic Description Reproductive traits Sexuality Species are classified as either gonochoric; gonochoric with rare (<1%) hermaphroditism; mixed sexuality with a regular incidence (>1%) of male, female, and hermaphroditic colonies; hermaphroditic; or parthenogenic Sex ratio For gonochoric species, the ratio of female to male colonies Mode of reproduction Species are classified as either a broadcast spawner; internal brooder; or an external surface brooder Maximum oocyte size The maximum oocyte size in terms of diameter, measured in µm Length of oogenic cycle Number of months required for completion of 1 oogenic cycle. Species with multiple concur- rent oogenic cycles and where length of a single cycle cannot be determined are classified accordingly Polyp fecundity Average number of mature oocytes per polyp Breeding period Number of months when spawning or brooding occurs per year Other factors Clade/Subclade Based on McFadden et al. (2006). See
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