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Early Development and Acquisition of Zooxanthellae in the Temperate Symbiotic Sea Anemone Anthopleura ballii (Cocks)
Abstract
The ova of Anthopleura ballii become infected with zooxanthellae (endosymbiotic dinoflagellates) of maternal origin just prior to spawning. After fertilization, the zygotes undergo radial, holoblastic cleavage, and then gastrulate by invagination to form ciliated planulae. Because the zooxanthellae are localized on one side of the ovum-and later, within the blastomeres at one end of the embryo-invagination leads to the zooxanthellae being restricted to the planular endoderm and hence to the gastrodermal cells of the adult anemone. We propose that maternal inheritance of zooxanthellae plays an important part in the success of these temperate sea anemones, which live in regions where potential sources of zooxanthellae are scarce.
... Furthermore, blastomeres containing zooxanthellae drop into the blastocoel during gastrulation, and zooxanthellae become restricted to the endoderm in the gastrula or early planula (Hirose et al ., 2000). In a temperate zooxanthellate sea anemone, Anthopleura ballii , blastomeres containing zooxanthellae were observed to invaginate at one end of the embryo, leading to the restriction of zooxanthellae to the planula endoderm (Davy and Turner, 2003). Thus, the larvae of these corals and this sea anemone do not transfer the algae from the ectoderm to the endoderm. ...
... This difference in timing may be related to the mode of gastrulation. However, in the temperate sea anemone Anthopleura ballii, which produces zooxanthellate eggs, zooxanthellae are localized at one end of the blastula, and the blastomeres containing zooxanthellae invaginate during gastrulation, restricting the zooxanthellae to the endoderm of planulae (Davy and Turner, 2003). The uneven distribu- tion of zooxanthellae in embryos could indicate an earlier determination of presumptive endodermal cells. ...
... We observed no degraded zooxanthella particles in the surface layer of embryos or early planulae of M. digitata. In contrast, Davy and Turner (2003) only occasionally found zooxanthellae in the ectoderm of the late gastrula or early planula and suggested that these stray zooxanthellae may degrade in the host or be expelled. It has been proposed that degraded zooxanthella particles are produced by partial digestion of zooxanthellae by the host (Titlyanov et al., 1996(Titlyanov et al., , 1998Mise and Hidaka, 2005). ...
We studied the early development of zooxanthellae-containing eggs of the scleractinian corals Porites cylindrica and Montipora digitata to elucidate how zooxanthellae become localized to the endoderm of planulae during the course of development. In both species, zooxanthellae were distributed evenly in the oocytes and delivered almost equally to the blastomeres during cleavage. In P. cylindrica, gastrulation occurred via delamination or ingression, and blastomeres containing zooxanthellae dropped into the blastocoel during gastrulation. Thus, zooxanthellae were restricted to the endodermal cells at the gastrula or early planula stage in P. cylindrica. In M. digitata, gastrulation occurred by a combination of invagination and epiboly to form a somewhat concave gastrula. Zooxanthellae were present in both endodermal and ectodermal cells of early planulae, but they disappeared from the ectoderm as the planulae matured. In our previous study on two species of Pocillopora, we found that zooxanthellae were localized in eggs as well as in embryos, and that blastomeres containing zooxanthellae later dropped into the blastocoel to become restricted to the endoderm (Hirose et al., 2000). The timing and mechanism of zooxanthella localization and types of gastrulation differed among species belonging to the three genera. These results suggest that zooxanthella localization in the embryos reflects the timing of the determination of presumptive endoderm cells and/or specificity of zooxanthellae toward presumptive endoderm cells.
... The modes in which the symbioses are established are variable, but they can be classified, broadly, in three categories: (i) vertical transmission (i.e. symbionts are transmitted directly from parent to offspring through eggs or embryos), as occurs with the zooxanthellae in some Anthozoa (Davy and Turner 2003); (ii) horizontal acquisition (i.e. from an adult to another, via non-hereditary mechanisms), as in macroparasites with complex life cycles (Cézilly et al. 2014); and (iii) environmental transmission, when the individual acquires the symbionts directly from the environmental stock (Gros et al. 1998). Previous studies have shown that either vertical or horizontal transmission enables the achievement of obligatory symbioses in marine invertebrates (Avila and Carballo 2006;Padilla-Gamiño et al. 2012). ...
... We did not find any algal propagules inside D. janiae reproductive elements, although these are common in other marine invertebrates (e.g. corals; Davy and Turner 2003). No axial conceptacles (or sporangia) in the J. adhaerens living in association with H. caerulea were found by Carballo and Ávila (2004) either. ...
In the tropics, the marine sponge Dysidea janiae lives in obligatory symbiosis with the red macroalga Jania adhaerens. However, how this symbiosis is achieved, and how it influences the reproduction of the sponge is still unknown. We analysed the influence of environmental variables on the gametogenesis and embryogenesis of the sponge. We also investigated the histology of the reproductive propagules of the sponge over 3 years, aiming to understand how this symbiosis is established. Dysidea janiae is viviparous and gonochoristic, with a continuous but small reproductive effort. The reproductive dynamics of gametes and embryos were explained by different sets of environmental variables. Although the temperature was not directly related to the reproduction of the sponge in general, there was an increase in the density of spermatic cysts during the year when the El Niño occurred. The day length was related to the embryo dynamics, which were interpreted as an indirect effect of the increase in photosynthetic rates of the symbiont on the energetic budget of the sponge. As no algal propagules were found associated with the eggs or larvae of the sponge, the acquisition of the algae by the sponge is probably a ‘trial-and-error’ relationship after larval release. We propose that the symbiosis increases the fitness of the adult sponge, forcing the larvae to seek new macroalgae to settle on and start a new symbiosis all over again.
... Relative to the wide array of developmental pathways displayed by actinians (Chia 1976;Fautin 1991), there is a general paucity of data on their spawning and subsequent embryonic development until metamorphosis (see reviews by Stephenson 1928Stephenson , 1935Mergner 1971;Campbell 1974;Spaulding 1974;Fautin et al. 1989). Investigations of shallow-water sea anemones mostly focused on early larval stages (e.g., Gemmill 1921;Fukui 1991;Weis et al. 2002;Davy and Turner 2003) with comparatively fewer publications on the development beyond the planula (Chia and Spaulding 1972;Spaulding 1972;Siebert 1973;Siebert and Spaulding 1976;Dunn 1977;Hand and Uhlinger 1992;Scott and Harrison 2008). Furthermore, substratum selectivity of planula larvae has been described for relatively few anthozoans, all of them from sublittoral areas (Gemmill 1921;Chia et al. 1989;Weis et al. 2002;Davy and Turner 2003;Scott and Harrison 2008). ...
... Investigations of shallow-water sea anemones mostly focused on early larval stages (e.g., Gemmill 1921;Fukui 1991;Weis et al. 2002;Davy and Turner 2003) with comparatively fewer publications on the development beyond the planula (Chia and Spaulding 1972;Spaulding 1972;Siebert 1973;Siebert and Spaulding 1976;Dunn 1977;Hand and Uhlinger 1992;Scott and Harrison 2008). Furthermore, substratum selectivity of planula larvae has been described for relatively few anthozoans, all of them from sublittoral areas (Gemmill 1921;Chia et al. 1989;Weis et al. 2002;Davy and Turner 2003;Scott and Harrison 2008). Settlement and metamorphosis in response to microbial films was reported in scleractinians (Negri et al. 2001;Webster et al. 2004), octocorals (Henning et al. 1991), and sea anemones (Scott and Harrison 2008), whereas planulae of two species of sea anemones were found to favour polychaete tubes (Chia and Spaulding 1972;Siebert 1974). ...
Sea anemones Allantactis parasitica Danielssen, 1890 (Actiniaria: Hormathiidae) living as epibionts on various gastropods were found at depths of similar to 725-1100 m off Labrador (eastern Canada). Live specimens collected with their hosts were studied in the laboratory to elucidate the role of the gastropod host in the reproductive and colonizing success of its actinian symbiont. Broadcast spawning occurred twice a year, in spring and late fall, in correlation with maximum phytoplankton or phytodetritus abundance, often during copulation of the gastropod hosts. The fully developed planula stage was reached after similar to 22 d. Settlement on the host's shell generally occurred 40-44 d postfertilization, although some larvae delayed settlement for up to 22 weeks in the absence of a host. Independent and pairwise settlement trials showed that shells of live bathyal gastropods were highly favoured compared with shells of shallow-water gastropods, empty shells, pebbles, or sand. Juveniles developed 24 tentacles and reached similar to 10 mm in basal disk diameter and similar to 12 mm in stalk height after 21 months of growth. The estimated growth rates of A. parasitica suggest that symbiotic individuals would require 6-7 years to reach the mean maximum adult size (similar to 35 mm, basal disk diameter), whereas asymbiotic individuals would need 11-12 years.
... These dinoflagellates typically reside within the cells of the host cnidarian's gastrodermis (i.e., the innermost tissue layer that borders the gastrovascular cavity), where they are bound by a membrane complex consisting of a series of membranes of algal origin plus an outermost hostderived membrane (184,389); this entire entity is referred to as the symbiosome. The dinoflagellates can be acquired by maternal inheritance (79) or, more commonly, anew with each generation from the surrounding seawater (12) when they must invade their host and form a functional partnership in order to persist. ...
... This indicates that there are modes of invasion other than phagocytosis of algae after entry into the gastrovascular cavity. Mechanisms of symbiont sequestration into germ cells or developing embryos that occurs in cnidarian species that undergo vertical symbiont transmission is also very poorly understood (24,79). Symbiodinium acquisition by or invasion of cnidarian hosts is an obvious area that needs substantial further study. ...
The symbiosis between cnidarians (e.g., corals or sea anemones) and intracellular dinoflagellate algae of the genus Symbiodinium is of immense ecological importance. In particular, this symbiosis promotes the growth and survival of reef corals in nutrient-poor tropical waters; indeed, coral reefs could not exist without this symbiosis. However, our fundamental understanding of the cnidarian-dinoflagellate symbiosis and of its links to coral calcification remains poor. Here we review what we currently know about the cell biology of cnidarian-dinoflagellate symbiosis. In doing so, we aim to refocus attention on fundamental cellular aspects that have been somewhat neglected since the early to mid-1980s, when a more ecological approach began to dominate. We review the four major processes that we believe underlie the various phases of establishment and persistence in the cnidarian/coral-dinoflagellate symbiosis: (i) recognition and phagocytosis, (ii) regulation of host-symbiont biomass, (iii) metabolic exchange and nutrient trafficking, and (iv) calcification. Where appropriate, we draw upon examples from a range of cnidarian-alga symbioses, including the symbiosis between green Hydra and its intracellular chlorophyte symbiont, which has considerable potential to inform our understanding of the cnidarian-dinoflagellate symbiosis. Ultimately, we provide a comprehensive overview of the history of the field, its current status, and where it should be going in the future.
... Previous studies demonstrated that the Cnidaria-Symbiodiniaceae association is not stochastic, but mostly determined by host phylogeny and geography [77,78]. The coral genera that were found to maintain only a single Symbiodiniaceae species begin hosting more species with increase in latitude [48,79]. ...
Symbiotic relationships are very important for corals. Abiotic stressors cause the acclimatization of cell membranes in symbionts, which possess different membrane acclimatization strategies. Membrane stability is determined by a unique lipid composition and, thus, the profile of thylakoid lipids can depend on coral symbiont species. We have analyzed and compared thylakoid lipidomes (mono- and digalactosyldiacylglycerols (MGDG and DGDG), sulfoquinovosyldiacylglycerols (SQDG), and phosphatidylglycerols (PG)) of crude extracts from symbiotic reef-building coral Acropora sp., the hydrocoral Millepora platyphylla, and the octocoral Sinularia flexibilis. S. flexibilis crude extracts were characterized by a very high SQDG/PG ratio, a DGDG/MGDG ratio < 1, a lower degree of galactolipid unsaturation, a higher content of SQDG with polyunsaturated fatty acids, and a thinner thylakoid membrane which may be explained by the presence of thermosensitive dinoflagellates Cladocopium C3. In contrast, crude extracts of M. platyphylla and Acropora sp. exhibited the lipidome features of thermotolerant Symbiodiniaceae. M. platyphylla and Acropora sp. colonies contained Cladocopium C3u and Cladocopium C71/C71a symbionts, respectively, and their lipidome profiles showed features that indicate thermotolerance. We suggest that an association with symbionts that exhibit the thermotolerant thylakoid lipidome features, combined with a high Symbiodiniaceae diversity, may facilitate further acclimatization/adaptation of M. platyphylla and Acropora sp. holobionts in the South China Sea.
... Symbionts can be inherited vertically if they are already inside the oocyte, or horizontally at the larval stage or later on, after the metamorphosis. In corals, symbionts transmission varies between species(Simon K. Davy and Turner 2003). The symbiosis offers a shelter, inorganic nutrients from metabolic waste of the host and access to light for the algae. ...
The linearity of eukaryotic chromosomes requires the presence of a particular terminal chromatin structure, named telomere, to control the stability and function of genomes. Changes in telomere structure during life can determine longevity, stress resistance and disease susceptibility. Our knowledge on the contribution of environmental factors on telomere length (TL) variability remains at its infancy, as well as the diversity of telomere maintenance mechanisms and ageing strategies existing in the tree of life. In this regard reef building corals are an interesting but yet poorly investigated model to tackle the question of telomere response to environment. Indeed those long lived animals cannot escape external environmental stressors due to their fixed life mode nor internal ones due to the symbiosis, within their gastrodermal cells, with a photosynthetic microalgae. Here I combined an extensive field case study on 3 coral genera (two scleractinians, Pocillopora sp. and Porites sp. and the hydrozoan Millepora sp.) as well as controlled conditions test on the coral model Stylophora pistillata to unravel the possible links between telomere DNA length variation and environmental stress. I found that an absence of TL shortening with age and size in all the investigated corals. I observed a possible impact of dark induced bleaching on TL and different TL dynamics in wild populations. Pocillopora sp. mean TL is constrained both by genetic and environment while Porites sp. has a remarkable ability to maintain its TL regardless of size, genetic and some environment disturbance. Yet both of genera TLs were negatively correlated with seasonal deviations, identifying this environmental parameter as a factor overcoming TL maintenance in genera with different TL dynamics and life-history strategies.
... North Sea Actinia equina Sexual, asexual reproduction Chia and Rostron (1970) English Channel Cereus pedunculatus Sexual reproduction Rossi (1975) English Channel Actinia equina var. mesembryanthemum Sexual, asexual reproduction, brooding Carter and Thorp (1979) North Sea Actinia equina Asexual reproduction, brooding Gashout and Ormond (1979) North Atlantic Ocean Actinostola spetsbergensis Sexual reproduction, brooding, larva development Riemann-Zürneck (1976a, 1976b French Hummel and Bogaards (1991) Porcupine Abyssal Plain Amphianthus inornata Sexual, asexual reproduction Bronsdon et al. (1993) Porcupine Abyssal Plain Kadosactis commensalis Lough Hyne Anthopleura ballii Sexual reproduction, embryo development Davy and Turner (2003) North Atlantic Ocean Allantactis parasitica Sexual reproduction, larvae development Mercier and Hamel (2009) Gulf of Maine Metridium senile Sexual reproduction Lombardi and Lesser (2010) North Atlantic Ocean Urticina felina Brooding Mercier et al. (2011) ...
Our understanding of how sea anemones reproduce in the equatorial Central Indo‐Pacific region remains poor compared to other marine regions. Here we report the gametogenic cycles of Phymanthus pinnulatus, a zooxanthellate sea anemone found throughout the Indo‐Pacific tropics. Observations were based on 41 individuals collected in Singapore. We found P. pinnulatus to be gonochoric, with an equal sex ratio of 1:1. Phases of oogenesis and spermatogenesis were detailed for the first time in P. pinnulatus, and were consistent with phases in other actiniarians. Females with pedal disc diameters <10 mm were found to asynchronously produce oocytes. We also found that trophonemata were associated with both oocytes and spermaries during gametogenesis. In Singapore, the periods during which gametes matured in each sex of P. pinnulatus appeared to overlap. We were unable distinguish whether spawning was annual or continuous in P. pinnulatus. Our observations on the occurrence of maturing and matured gametes in P. pinnulatus were similar to those reported for other species within the Central Indo‐Pacific. It also coincided with the multispecies spawning of scleractinian corals in Singapore. This study contributes to the growing body of work focused on the biology of tropical actiniarians in the Central Indo‐Pacific region.
... Symbiotic dinoflagellates of the Symbiodiniaceae family are usually located inside the gastrodermis cells of the coelenterate host organism (i.e., in the innermost tissue layer that borders the gastrovascular cavity), where they are bound by a membrane complex that consists of the membrane of algal origin and the outer membrane of the animal host organism [24,25]. Zooxanthellae can be inherited [26] or, most often, captured from the environment [27]. ...
Numerous species of coral polyps form the structural basis of tropical coral reefs. Coral polyp tissues are rich in lipids. Currently, information on the composition of fatty acids and classes of coral lipid is reviewed. However, each lipid class represents a complex spectrum of molecular species of lipids, which is defined as the lipidome of a biological system. Scientific publications on human and higher terrestrial animal lipidomes exceed those on the lipidome of marine organisms by two orders of magnitude, and the data on coral lipidomes are very scattered. The existence of symbiotic coral species is completely dependent on the presence of intracellular microalgae (zooxanthellae), the loss of which is called coral bleaching and leads to the death of the entire coral reef. The bleaching causes significant changes in the lipid profile of corals. This paper summarizes information on the composition of common lipids, fatty acids, and molecules of polar and nonpolar lipid classes of octocoral and hexacoral polyps and their symbionts. We discuss general mechanisms of coral bleaching and show the importance of lipid indicators in the study of this process. The transition from classical integral indicators to the lipidomic analysis opens up new possibilities in the study of biochemistry and ecology of corals.
... The accepted cells then transition into a haploid vegetative state and are stored in the host's endodermal cells (Davy & Turner 2003;. Regulatory mechanisms are enforced to keep symbiont density at a relatively constant level, achieving dynamic stability by balancing population numbers through nutrient limitation and removal of excess algae (Muscatine & Pool 1979;Jones & Yellowlees 1997;Koike et al. 2004). ...
Mass bleaching events induced by climate change are threatening coral reef ecosystems worldwide. Elevated seawater temperatures cause breakdown of the coral’s endosymbiotic relationship with dinoflagellate algae from the genus Symbiodinium. Corals rely on these symbionts for the majority of their metabolic carbon (provided by photosynthetic products) and for efficient nitrogen cycling in the reef ecosystem. Researchers have predicted that corals may potentially adapt to higher ocean temperatures according to the Adaptive Bleaching Hypothesis (ABH), which states that bleaching can facilitate a change in symbiont communities, allowing more thermally tolerant symbionts to become dominant. Hosting thermally tolerant symbionts thus grants the coral a higher resistance to bleaching. However, confidence in this adaptation method has wavered due to the nutritional impairments of hosts harbouring thermally tolerant symbionts under normal environmental conditions. It is also unknown if coral species that do not currently associate with thermally tolerant symbionts would be able to successfully switch their symbiont communities. Here, I explore the mechanisms driving nutritional exchange in the symbiosis and determine the effect of establishing a non-native (heterologous) association with a thermally tolerant symbiont. A combined approach of bioinformatic analysis with proteomic and isotopic labelling experiments is used to uncover a link between host-symbiont cellular integration, the potential for nutrient exchange, and the success of establishing a symbiosis.
In Chapter 2, I characterized membrane protein sequences discovered in publicly available cnidarian and Symbiodinium transcriptomes and genomes to identify potential transporters of sugars into cnidarian cells and nitrogen products into Symbiodinium cells. I examined the facilitated glucose transporters (GLUT), sodium/glucose cotransporters (SGLT), and aquaporin (AQP) channels in the cnidarian host as mechanisms for sugar uptake, and the ammonium and high-affinity nitrate transporters (AMT and NRT2, respectively) in the algal symbionts as mechanisms for nitrogen uptake. Homologous protein sequences were used for phylogenetic analysis and tertiary structure deductions. In cnidarians, I identified putative glucose transporters of the GLUT family and glycerol transporting AQP proteins, as well as sodium monocarboxylate transporters and sodium myo-inositol cotransporters homologous to SGLT proteins. I predict that cnidarians use GLUT proteins as the primary mechanism for glucose uptake, while glycerol moves into cells by passive diffusion. I also identified putative AMT proteins in several Symbiodinium clades and putative NRT2 proteins only in a single clade. I further observed a high expression of putative AMT proteins in Symbiodinium, which may have resulted from adaptations to conditions experienced inside the host cell. This study is the first to identify transporter sequences from a diversity of cnidarian species and Symbiodinium clades.
The phylogenetic patterns seen in chapter 2 led to the hypothesis that symbiont types may have different influences on host-symbiont cellular integration. In chapter 3, I explored this notion using the model cnidarian Aiptasia. A population of anemones was rendered aposymbiotic using a menthol-bleaching method developed by my colleagues and I, and anemones then experimentally infected with either the native (homologous) symbiont (Symbiodinium minutum, clade B1) or a thermally tolerant heterologous symbiont (Symbiodinium trenchii, clade D1a). The response of the host proteome to these associations was examined by analysing the extracted host proteins with liquid chromatography-nano-electrospray-tandem mass spectrometry (LC-nano-ESI-MS/MS), and identifying resulting peptides against a cnidarian database. Proteins were compared between B1-colonised anemones, D1a-colonised anemones, and aposymbiotic anemones to determine which proteins were affected by the different treatments. Overall, I found that the response of D1a-colonised anemones mimicked that of aposymbiotic anemones to some degree, and showed signs of less efficient carbon and nitrogen pathways. Additionally, I discovered that the symbiosome protein NPC2 was upregulated only in B1-colonised anemones and could therefore be an important determinant of symbiont success.
I further investigated the apparent inadequacy of carbon and nitrogen pathways in hosts harbouring Symbiodinium D in chapter 4, using isotope labelling and sub-cellular imaging. Carbon and nitrogen fluxes between experimentally infected Aiptasia with both homologous (Symbiodinium B1) and heterologous (Symbiodinium D1a) symbionts were compared over multiple time points during symbiosis establishment. This was accomplished by incubating anemones in 13C- and 15N-labelled seawater to measure metabolite transfer to the host, and anemones were also fed 13C- and 15N-labelled Artemia to measure reverse translocation to the symbiont. Carbon and nitrogen enrichment in host tissues and symbiont cells were imaged using nanoscale secondary ion mass spectrometry (nanoSIMS). In both the earlier stages of symbiosis establishment (2 days post-inoculation) and later stages of symbiont proliferation (14 days post-inoculation), Symbiodinium B1 reached significantly higher population densities (> 300%) than Symbiodinium D1a. Differences in symbiont nitrogen uptake from host tissues were detectable, however they were likely due to nitrogen limitation imposed by the comparatively high densities of the homologous symbiont. While Symbiodinium B1 cells maintained a high degree of carbon fixation throughout symbiosis establishment, less than 50% of Symbiodinium D1a cells were found to be fixing carbon in the later stages of establishment, despite still receiving substantial amounts of host-derived nitrogen. These findings support my previous prediction that Symbiodinium D1a affects the host’s carbon and nitrogen pathways, acting as a less mutually beneficial symbiont.
Overall, my results provide new insights into the underlying factors determining the success of symbiotic interactions. The results indicate that cnidarian hosts and their dinoflagellate symbionts have adapted to the symbiotic life-style by cellular integration, thereby making compatibility of certain biological processes a key factor in determining symbiosis success. Furthermore, the findings presented here show how the potential for nutritional exchange may be linked to host-symbiont compatibility and hence specificity. This information is relevant when making predictions about which corals may successfully adapt to climate change via the ABH.
... Its shape varies significantly: it can be spherical, flattened, or folded (Gemmill, 1920;Fukui, 1991;Fritzenwanker et al., 2007). Gastrulation in this case proceeds either by classical invagination (Nyholm, 1943;Spaulding, 1974;Davy and Turner, 2003;Fritzenwanker et al., 2004;Kraus and Technau, 2006;Magie et al., 2007) or by the combination of invagination and unipolar immigration of cells from the archenteron apex (see, e.g., (Fukui, 1991)). ...
The data revealed by comparative embryology of the basal (diploblastic) metazoans is traditionally considered a valuable potential source of information on the origin and early evolution of the animal kingdom and its major clades. Special attention is paid to the fundamental morphogenetic process of gastrulation during which the cells of the early embryo differentiate into the germ layers and the primary body plan is formed. Comparative analysis of gastrulation in different cnidarian taxa reveals high level of intergroup, intragroup, and individual variation. With few exceptions, there is no robust correlation between the type of gastrulation and the taxon. Current data do not support the idea that morphogenetic processes underlying cnidarian gastrulation can be divided into several distinct types. Rather, there is a continuum of equifinal ontogenetic trajectories. In cnidarians, the mode of gastrulation apparently depends less on the macroevolutionary history of the species than on various evolutionary plastic features, such as the oocyte size, the amount of yolk, the number of cells at the blastula (or morula) stage, the presence of phototrophic symbionts, or the ecology of the larva. Thus, in cnidarians, morphogenetic basis of gastrulation contains only a very weak phylogenetic signal and can have only limited application in phylogenetic reconstructions. On the other hand, comparative studies of the ontogeny of the basal metazoans shed light on the general rules of the evolution of morphogenetic processes that is crucial for understanding the early history of the animal kingdom.
... Todos estes, no entanto, dependem de uma relação de simbiose com dinoflagelados fotossintetizantes para o desempenho perfeito do papel de construtores. Estes simbiontes pertencem ao gênero Symbiodinium e são mais conhecidos como zooxantelas [2]. A partir desse contexto, temos duas divisões genéricas: cnidários zooxantelados e azooxantelados [3,4]. ...
Introdução O Filo Cnidaria tem cerca de 20 representantes no Brasil que podem contribuir ativamente para a construção de recifes de coral, desses, a maior parte é de corais escleractínios e o restante de hidróides calcários [1]. Todos estes, no entanto, dependem de uma relação de simbiose com dinoflagelados fotossintetizantes para o desempenho perfeito do papel de construtores. Estes simbiontes pertencem ao gênero Symbiodinium e são mais conhecidos como zooxantelas [2]. A partir desse contexto, temos duas divisões genéricas: cnidários zooxantelados e azooxantelados [3,4]. Essa denominação implica numa série de fatores ecológicos, bióticos e abióticos, inerentes à manutenção da relação coral x zooxantela, tais como temperatura e intensidade luminosa, que são influenciados diretamente pela profundidade. Uma vez que zooxantelas são fotossintetizantes, é de se inferir que os organismos aos quais elas se associam se distribuam em locais rasos, de pouca sedimentação e de luminosidade e temperatura elevadas, ou seja, ambientes recifais. Por conseguinte, todos os cnidários construtores de recifes de águas rasas são zooxantelados [1]. E, em se tratando desses ecossistemas, é essencial que esses organismos sejam bastante tolerantes a grandes variações ambientais. No entanto, nos últimos anos, a frágil e relativa estabilidade mantida nos ambientes recifais vêm sendo ameaçada por alterações ambientais resultantes da ação antrópica, como o aquecimento global, em grande escala, e a eutrofização de ambientes costeiros, como degradações mais pontuais [5]. Mais recentemente, pesquisas com finalidades comerciais e científicas têm sido realizadas, visando uma maior e melhor exploração de recursos em águas profundas ao redor do mundo, uma vez que seus habitantes são menos afetados por mudanças climáticas (mesmo sendo vítimas de degradação via atividades pouco regulamentadas) [3,6]. No Brasil, apesar de os esforços nesse sentido ainda serem poucos [4,7], algumas expedições oceanográficas, resultantes de parcerias do Governo Federal, Marinha do Brasil e instituições de pesquisa têm contribuído para uma melhor compreensão da biodiversidade desses ambientes. Tendo em mente a estabilidade desses ambientes profundos, assim como a necessidade de preservação de corais zooxantelados para a futura construção e manutenção do arcabouço de ecossistemas recifais em águas rasas, o objetivo do presente trabalho é, portanto, reportar a ocorrência de corais e hidróides calcários zooxantelados em ambientes de profundidade no nordeste do Brasil.
... Similarly, it remains unclear why no embryos of Markuelia species in the gastrula stage and in the stages prior to the prehatching form have been discovered. Perhaps the former is due to a short time span during which gastrulation lasted, a phenomenon that is seen in some living invertebrates (Davy and Turner, 2003). ...
Extraordinarily rare phosphatized embryos liberated from fossiliferous limestone of the Middle Cambrian (about 500 Myr old) Gaotai Formation of Duyun, southern China, are assigned to Markuelia qianensis n. sp. Several specimens with increasing numbers of blastomeres may represent four successive cleavage stages, seemingly exhibiting a radial holoblastic cleavage pattern. No subsequent stages showing gastrulation were observed. However, several specimens are late, pre-hatching stages, each with a vermiform shape coiled in either left-or right-handed directions within the fertilization envelope. These specimens indicate that the intuitively assumed difference in preservation potential between early cleavage and late pre-hatching stages is probably not valid. This new material clarifies the affinity of the first fossilized invertebrate embryos ever described, from the same rocks, which were originally attributed to arthropods, presumably trilobites. Instead, they belong to scalidophorans, and this finding infers likely diversified cleavage patterns for stem members of this group, and yields fresh insight into the embryogenesis of early metazoans as a whole.
... Symbiodinium has been shown to be either directly inherited from parent to offspring during sexual reproduction or by each generation acquiring a new complement of symbionts from the external environment at some stage of the life cycle of the host (Trench 1979). Examples of direct inheritance of Symbiodinium are found principally among the cnidarians (Trench 1987;Davy and Turner 2003), whereas examples of acquisition of the symbionts from the external environment are found among cnidarians, platyhelminths, and mollusks (Trench 1987) including the bivalves Corculum cardissa (Kawaguti 1950;Farmer et al. 2001) and Tridacna spp. as well as nudibranchs (Kempf 1984). These symbionts may be acquired prior to metamorphosis or after (Kempf 1984). ...
The importance of the dinoflagellate Symbiodinium sp. was studied in the early life stages of the gastropod Strombus gigas. This dinoflagellate was not found in the eggs or the gelatinous mass surrounding the eggs of the mollusk; therefore, Symbiodinium is not inherited directly. To determine whether the planktonic veligers can acquire these algae from the environment, they were exposed to freshly isolated Symbiodinium from adult S. gigas (homologous). The optimal stage for Symbiodinium inoculation was found at 48 h post-hatching. Survival and growth rates of veligers and juveniles were higher when inoculated with freshly isolated Symbiodinium in conjunction with daily feeding of Isochrysis spp. Veligers inoculated with Symbiodinium freshly isolated from three host species elicited distinct responses: (1) veligers did not take up Symbiodinium isolated from the hydrozoan Millepora alcicornis suggesting that there is discrimination on contact prior to ingestion, (2) veligers did take up Symbiodinium isolated from the anemone Bartholomea annulata, but the algae did not persist in the host tissue suggesting that selection against this type took place after ingestion or that the algae did not divide in the host, and (3) veligers did take up Symbiodinium isolated from Pterogorgia anceps where it persisted and was associated with metamorphosis of the larvae. In contrast, the Symbiodinium freshly isolated from S. gigas were not associated with metamorphosis and required an inducer such as the red alga Laurencia poitei. These data present a significant advancement for the establishment of a new approach in the aquaculture of this important but declining Caribbean species.
... On the other hand, in temperate waters, anthozoanÁsymbiotic dinoflagellate symbioses seem to be more stable, and the mechanism of maternal symbiont transmission appears to be predominant (Muller-Parker and Davy 2001;Davy and Turner 2003). Davy et al. (1997) pointed out that a predominance of vertical transmission (maternally) of zooxanthellae at high latitudes could relate to a scarcity of potential donors and selection against hosts with horizontal (indirect) transmission mechanisms. ...
The actiniarian sea anemone, Entacmaea quadricolor, and the scleractinian coral, Alveopora japonica, host symbiotic dinoflagellates belonging to the genus Symbiodinium (Freudenthal). We studied the host–symbiont specificity of these two anthozoan hosts in the northwestern Pacific Ocean. Symbionts within the two hosts were identified using partial large subunit (LSU) ribosomal DNA (rDNA) and complete internal transcribed spacers (ITS) 1 rDNA regions. The host, E. quadricolor, was identified using the partial LSU rDNA molecular marker. Genetic analysis showed that E. quadricolor only harbors dinoflagellates belonging to subclade C1/3 of the genus Symbiodinium. Moreover, no genetic variation was detected among the symbionts of E. quadricolor within the study region (Korea and Japan), even though the two distant sites were separated by more than 1000 km, at collection depths of 1 m in shallow and 13–16 m in deep water. Whilst scleractinian corals host multiple Symbiodinium clades in tropical waters, A. japonica, sampled over a wide geographical range (800 km) within the study region, only hosts Symbiodinium sp. clade F3. The high specificity of endosymbionts in E. quadricolor and A. japonica within the northwestern Pacific Ocean could be accounted for because symbiotic dinoflagellates within the host anemones appear to be acquired maternally, and the Kuroshio Current might affect the marine biota of the northwestern Pacific. However, the consistency of the symbiotic relationships between these two anthozoan hosts and their endosymbionts could change after climate change, so this symbiotic specificity should be monitored.
... The presence of zooxanthellae may represent an advantage for the hydroid providing a higher competitive ability and favouring its wide diffusion. Acquisition of zooxanthellae in tropical coral symbioses is mainly from the surrounding waters rather than from maternal inheritance, whereas transmission patterns in tem- perate symbioses have been rarely identified (Davy & Turner, 2003). In hydrozoans, both zooxanthellate euden- driids (E. ...
Eudendrium moulouyensis is a zooxanthellate hydroid originally described from the Chafarinas Islands (Alboran Sea, south-western Mediterranean) in summer 1991. According to the original description, this species can be identified due to the occurrence of symbiotic zooxanthellae in the entire endodermal layer of the colony (gastrodermis and tentacle endodermis), a unique feature among the Mediterranean Eudendrium species. However, several aspects of its life cycle and the extent of its phenotypical variability are still unknown. Since winter 2004, colonies of E. moulouyensis were recorded throughout the year from 0.5 m to 30 m depth from the southern Adriatic Sea (Otranto Channel) and the Gibraltar Strait (Alboran Sea). Additional specimens were collected from the northern Adriatic (Vis, Croatia), Sicily Channel (Pantelleria and Lampedusa Islands), and western Sardinia (Costa Paradiso). These findings offered the opportunity to describe for the first time the full life cycle and to elucidate several biological aspects related to phenotypical variation of colony morphology, vertical zonation, seasonality, zooxanthellae–polyp relationship, and cnidome morphology and distribution. The number and morphology of male gonophores per reproductive polyp is described here for the first time, providing a useful taxonomic character to easily discriminate Myrionema amboinense from E. moulouyensis. From the available information, the occurrence of M. amboinense in the Mediterranean Sea should be regarded as doubtful, if they are not accompanied by observations of cnidome, male gonophores or distinctly separate tentacles whorls.
... Endosymbiotic zooxanthellae are not restricted in occurrence to scleractinian corals [15,16] and are found in bivalves (e.g. Tridacna gigas [17,18], scyphozoans (e.g., Cassiopea xamachana; [19,20]), and flatworms (e.g., Amphiscolops sp [21]), as well as in other cnidarians, such as sea anemones [Anthopleura ballii [22]). One marine group in which they may be commonly found is the Octocorallia. ...
Increases in Sea Surface Temperatures (SSTs) as a result of global warming have caused reef-building scleractinian corals to bleach worldwide, a result of the loss of obligate endosymbiotic zooxanthellae. Since the 1980's, bleaching severity and frequency has increased, in some cases causing mass mortality of corals. Earlier experiments have demonstrated that zooxanthellae in scleractinian corals from three families from the Great Barrier Reef, Australia (Faviidae, Poritidae, and Acroporidae) are more sensitive to heat stress than their hosts, exhibiting differential symptoms of programmed cell death - apoptosis and necrosis. Most zooxanthellar phylotypes are dying during expulsion upon release from the host. The host corals appear to be adapted or exapted to the heat increases. We attempt to determine whether this adaptation/exaptation occurs in octocorals by examining the heat-sensitivities of zooxanthellae and their host octocoral alcyonacean soft corals - Sarcophyton ehrenbergi (Alcyoniidae), Sinularia lochmodes (Alcyoniidae), and Xenia elongata (Xeniidae), species from two different families. The soft coral holobionts were subjected to experimental seawater temperatures of 28, 30, 32, 34, and 36°C for 48 hrs. Host and zooxanthellar cells were examined for viability, apoptosis, and necrosis (in hospite and expelled) using transmission electron microscopy (TEM), fluorescent microscopy (FM), and flow cytometry (FC). As experimental temperatures increased, zooxanthellae generally exhibited apoptotic and necrotic symptoms at lower temperatures than host cells and were expelled. Responses varied species-specifically. Soft coral hosts were adapted/exapted to higher seawater temperatures than their zooxanthellae. As with the scleractinians, the zooxanthellae appear to be the limiting factor for survival of the holobiont in the groups tested, in this region. These limits have now been shown to operate in six species within five families and two orders of the Cnidaria in the western Pacific. We hypothesize that this relationship may have taxonomic implications for other obligate zooxanthellate cnidarians subject to bleaching.
... can acquire their symbionts in a number of ways, including from the surrounding water column and by infection of the ova prior to their release (Davy & Turner 2003). Broadcast spawning is the dominant reproductive mechanism of corals, (~85%) (Schwarz et al. 2002) and occurs as a synchronous event (Harrison et al. 1984). ...
Many corals live in marginal habitats, close to their survival thresholds of water temperature, light penetration and aragonite saturation. Living under these highly variable and extreme conditions is likely facilitated by specific physiological adaptations and/or the presence of unique species of coral and their symbionts but
data on these factors are limited. The specific objectives of the study were to: (1) examine the diversity and distribution patterns of corals in marginal environments, (2) investigate the diversity, distribution patterns and host specificity of symbionts in corals in marginal
environments, (3) assess the influence of environmental variables on host and symbiont distribution in marginal environments, in comparison to 'optimal' environments, and (4) examine the physiological responses to changing
environmental conditions and stress of corals and their symbionts in marginal environments. Surveys of coral community patterns were conducted at the Kermadec Islands (KI), New Zealand, and Palmyra Atoll, USA, with local scale environmental parameters (i.e. wave exposure and sedimentation) found to control the diversity and distribution of the coral communities. Symbiodinium types were identified to subcladal
level in a range of coral species at each of the survey sites, using ITS2-DGGE. A high diversity of C type symbionts (19 types in 13 host genera), and reduced host specificity was observed at the high latitude site of Lord Howe Island (LHI),
Australia, with similarly high diversity at the KI (10 types in 9 genera). Thirteen novel clade C types were identified in corals at LHI, with two of these types also present in hosts at the KI. The reduced host specificity of symbionts at LHI, compared to tropical sites, implies that the evolution of novel holobionts may be an important mechanism whereby corals can cope with variable and stressful conditions. Further, physiological assessment of the novel LHI symbionts led to the suggestion that Symbiodinium at LHI may be specialised for cooler and more variable
temperatures, so contributing to the success of corals at this marginal location. In contrast, a low diversity of generalist symbionts (C and D types) were uncovered at the equatorial site of Palmyra Atoll (10 types in 13 genera), attributed to the stressful environmental regime resulting in a reduced population of stresstolerant symbionts. The variation in environmental parameters, particularly sedimentation, around Palmyra Atoll has led to diversification of coral communities,
however this environmental variation has not affected the symbiont communities. While it has been suggested that marginal coral communities might be better adapted for survival in an environment modified by global climate change, the local scale environmental factors are also important drivers of both coral and symbiont
distributions, and should be considered when making predictions for the future. Further, assessment of the physiological tolerance ranges of both the multiple, novel symbionts at high latitudes, and the few, potentially stress-tolerant symbionts at Palmyra should be conducted, to help determine whether they have the ability to
adjust to new environmental conditions.
... The Wnal stages of metamorphosis, which result in the formation of a juvenile polyp typically take place after attachment to the substratum (Riemann-Zürneck 1976). Previous studies on larval settlement of broadcastspawning or brooding sea anemones have sometimes had problems with achieving settlement and metamorphosis of the planulae (Gemmill 1921; Chia et al. 1989; Weis et al. 2002; Davy and Turner 2003). This most likely indicates sub-optimal settlement conditions such as inappropriate settlement substrata or lack of important metamorphosis cues (Harrison and Wallace 1990; Miller and Mundy 2003). ...
Sea anemones that host obligate symbiotic anemonefish are ecologically important throughout many coral reef regions of the Indo-Pacific. This study provides the first quantitative data on larval settlement rates and juvenile development of two species of host sea anemone, Heteractis crispa and Entacmaea quadricolor. Larvae were reared from broadcast spawned gametes of sexually reproductive male and female anemones collected from the Solitary Islands Marine Park, NSW, Australia. Prior to the start of the experiments, H. crispa larvae were reared for 3 days after spawning in March 2004 and E. quadricolor larvae were reared for 4 days after spawning in February 2005. Larval settlement onto biologically conditioned terracotta tiles in outdoor flow-through seawater aquaria was first recorded 4 days after spawning for H. crispa and 5 days after spawning for E. quadricolor. Peak settlement occurred 10 days after spawning, with a mean of 33.4 and 50.3% of the original groups of 350 larvae in replicate tanks settling for H. crispa and E. quadricolor, respectively. Tentacles arose as outpocketings of the oral region, at first appearing as small rounded buds. These buds elongated to form long, thin, tapering tentacles in H. crispa, whereas E. quadricolor tentacles had slight bulbs below the tips. Juvenile anemones, especially H. crispa, were found to have very different colouration and markings when compared with adult anemones, and therefore the descriptions and images provided here will enable correct identification of juvenile recruits.
... β-Tubulin is shown as a loading control. the distribution of pigment granules (Tessier, 1931); the polar localization of symbiotic dinoflagellates in corals and sea anemones (Davy and Turner, 2003; Hirose et al., 2000; Marlow and Martindale, in press); and the asymmetric distribution of protein, such as Dsh in Nematostella (this study), or mRNAs such as Wnt and Tcf in Hydractinia (Plickert et al., 2006), Cnox4-Pc and Brachyury in Podocoryne (Spring et al., 2002; Yanze et al., 2001), and CheFz1 and CheFz3 in Clytia (Momose and Houliston, 2007). Of these asymmetrically localized factors in cnidarian eggs, only CheFz1 and CheFz3 in Clytia have been shown to be causally involved in patterning along the oral aboral axis. ...
The relationship between egg polarity and the adult body plan is well understood in many bilaterians. However, the evolutionary origins of embryonic polarity are not known. Insight into the evolution of polarity will come from understanding the ontogeny of polarity in non-bilaterian forms, such as cnidarians. We examined how the axial properties of the starlet sea anemone, Nematostella vectensis (Anthozoa, Cnidaria), are established during embryogenesis. Egg-cutting experiments and sperm localization show that Nematostella eggs are only fertilized at the animal pole. Vital marking experiments demonstrate that the egg animal pole corresponds to the sites of first cleavage and gastrulation, and the oral pole of the adult. Embryo separation experiments demonstrate an asymmetric segregation of developmental potential along the animal-vegetal axis prior to the 8-cell stage. We demonstrate that Dishevelled (Dsh) plays an important role in mediating this asymmetric segregation of developmental fate. Although NvDsh mRNA is ubiquitously expressed during embryogenesis, the protein is associated with the female pronucleus at the animal pole in the unfertilized egg, becomes associated with the unipolar first cleavage furrow, and remains enriched in animal pole blastomeres. Our results suggest that at least one mechanism for Dsh enrichment at the animal pole is through its degradation at the vegetal pole. Functional studies reveal that NvDsh is required for specifying embryonic polarity and endoderm by stabilizing beta-catenin in the canonical Wnt signaling pathway. The localization of Dsh to the animal pole in Nematostella and two other anthozoan cnidarians (scleractinian corals) provides a possible explanation for how the site of gastrulation has changed in bilaterian evolution while other axial components of development have remained the same and demonstrates that modifications of the Wnt signaling pathway have been used to pattern a wide variety of metazoan embryos.
... Cnidarians display numerous patterns of embryogenesis. Gastrulation, or the formation of the germ layers, may occur via invagination, ingression, delamination, or mixed patterns (Uchida and Yamada, 1968;Szmant-Froelich et al., 1980;Davy and Turner, 2003). As a model of primitive metazoan development, jellyfish and hydrae have been studied in depth and a large stock of information is available. ...
Embryogenesis in the reef building corals Acropora intermedia, A. solitaryensis, A. hyacinthus, A. digitifera, and A. tenuis was studied in detail at the morphological level, and the relationships among the animal pole, blastopore, and mouth were investigated for the first time in corals. These species showed essentially the same sequence of development. The embryo undergoes spiral-like holoblastic cleavage despite the presence of a dense isolecithal yolk. After the morula stage, the embryo enters the "prawn-chip" stage, which consists of an irregularly shaped cellular bilayer. The embryo begins to roll inward to form the bowl stage; the round shape observed during this stage suggests that it may be the beginning of gastrulation. However, the blastopore closes and the stomodeum (mouth and pharynx) is formed via invagination at a site near the closed blastopore. During the planula stage, a concavity forms in the aboral region in conjunction with numerous spirocysts, suggesting that spirocysts are used to attach to the substrate before the onset of metamorphosis.
The phylum Cnidaria contains an estimated 11 000+ living species and is almost exclusively an aquatic group, primarily marine but with some freshwater species and a few terrestrial parasitic species. Cnidarians reproduce both sexually and asexually, most species incorporating both methods. They produce gametes (eggs and sperm), can be monoecious, producing both eggs and sperm, or dioecious, with individuals of separate sexes (gonochoric). Cnidarians are soft‐bodied, diploblastic (two cell layers) metazoans (animal kingdom), with primary radial symmetry (although with some variations). Threats to cnidarians include climate change, infectious diseases, development of shorelines, increase in surface runoff, land‐based sources of pollution, ship groundings, and damaging fishing techniques (dynamite, nets, etc.). As a possible indicator of some of these detrimental changes, there has been an increase in the frequency of jelly blooms.
The giant Caribbean sea anemone, Condylactis gigantea, is an ecologically important member of the benthic community. It provides habitat for many species, including symbiotic cleaner shrimps, and is recognized by reef fishes as a cleaning station cue. Numbers of C. gigantea in Florida have recently declined, possibly due to deteriorating environmental conditions and increasing harvest pressure. A previous research finding indicating that C. gigantea spawns in the late spring has been questioned by fishers for the aquarium trade industry. We therefore examined specimens of C. gigantea collected monthly from October 2011 to September 2012 in the Florida Keys to characterize the reproductive cycle, also measuring several physical and chemical parameters of concurrently collected water samples. We ascertained that the anemone is gonochoric and has a 1:1 sex ratio. Within and between individuals, at the same time and place, spermatogenesis was synchronous, whereas oocyte development was asynchronous. Low-level spawning occurred between October and April with a peak in May, in good agreement with earlier research. Water quality at both sites showed no discernible change over the study period. Conservation efforts directed at population management could benefit this anemone.
The extent of salmon farming’s influence on the environment and the uptake of particulate and dissolved effluents by benthic organisms was assessed using community structure and stable isotope analyses. Sediment cores were collected along two directions: perpendicular to and in the direction of the main residual current, at 0, 25 and 200 m from two salmon farms (Millstone and Cranford) located in Mulroy Bay, Ireland. In addition, artificial substrates were placed for 2 months at 1 m depth at 0, 25 and 200m from one farm to trace the uptake of farm-related nutrients by fouling organisms. The extent of measurable change in benthic communities (abundance, diversity, structure, trophic composition) depended on residual current direction. Intra-specific variation in isotopic values in benthic invertebrates was mostly explained by distance from cages. Organisms collected at impacted sites exhibited a shift in isotopic composition towards that of farm wastes. A shift in δ13C was observed in several invertebrates, including the polychaetes Malacoceros fuliginosus and Nephtys hombergii, Nematoda and the anemone Anthopleura balii. Fouling communities collected on artificial structures, mainly composed of tunicates (Ascidiella aspersa) showed higher δ15N values at fish cage sites compared to 200 m sites. The study demonstrated that fish effluents were assimilated and became food sources for several native organisms. Keywords: aquaculture, organic matter, stable isotope, community structure, diet shift, trophic structure
Abstract While offspring size is a widely studied concept in evolutionary ecology, mechanisms affecting offspring phenotype in species with postzygotic parental care are incompletely understood. We examined the impact of sibling fusion on ontogenetic shifts in offspring size in the brooding sea anemone Urticina felina. Fusion occurred among brood-protected embryos in U. felina, whereas it occurred postrelease among settlers of corals studied here and previously. Two fusion products were evidenced: morphologically aberrant offspring and large homogeneous offspring coined "megalarvae." The frequent occurrence (∼77%) of megalarvae identifies them as the primary fusion product, which drove an increase in offspring size and within-clutch size variation before release. Lipid signatures suggest that morphologically aberrant juveniles represent by-products that do not reach adulthood. Not only were occurrences of megalarvae common in the populations studied, they increased with maternal fecundity, suggesting that sibling fusion may be a form of kin cooperation integral to the reproductive success of U. felina, warranting investigation in other live-bearing invertebrate taxa.
Kleptoplasty, the process by which a typically heterotrophic organism acquires and retains chloroplasts from a photosynthetic
organism, is quite widespread in ciliates, foraminifera and sacoglossans and variable in terms of longevity and functionality.
The sacoglossans are the only group of metazoans which have been shown to harbor functional plastids intracellularly. The
ability of the sea slug Elysia chlorotica to “steal” algal chloroplasts, retain them intracellularly, and then integrate the foreign organelles with the sea slug’s
metabolism allowing the animal to survive photoautotrophically for months, is unprecedented and for the most part, currently
unexplainable. Equally remarkable is the stability and adaptability of the chloroplasts; they not only survive the ingestion
process and resist digestion by the host, but they also adjust osmotically and metabolically to the entirely new cellular
environment devoid of any new protective membrane. The biochemistry of such an association is intriguing because of the evidence
supporting the reliance of normal chloroplasts on the nucleus to encode the great majority of their proteins and regulate
the expression of chloroplast encoded proteins. There appear to be no algal nuclei in E. chlorotica and the chloroplast genome of V. litorea does not have an unusual coding capacity to account for all of the nuclear encoded chloroplast targeted proteins necessary
to sustain the observed chloroplast activity. Preliminary results supporting lateral gene transfer are encouraging and exciting.
It is likely that a combination of organelle/protein stability and lateral gene transfer play key roles in sustaining this
fascinating association in sacoglossan molluscs.
In adult cnidarians, symbiotic dinoflagellate Symbiodinium are usually located in the gastrodermis. However, the onset of this endosymbiotic association and its regulation during larval
development are unclear. This study examined the distribution of the Symbiodinium population in tissue layers of planula larvae released from the stony coral Euphyllia glabrescens. Symbiodinium were redistributed from the epidermis to the gastrodermis, at a rate that was fastest during early planulation and then decreased
prior to metamorphosis. This process indicates that the endosymbiotic activity of coral tissues is developmentally regulated.
During the early larval stage, both the epidermis and gastrodermis contained Symbiodinium; then, as the larvae developed toward metamorphosis, the numbers in the epidermis gradually diminished until they were only
found in the gastrodermis. The mechanism of redistribution remains unknown, but may be due to a direct translocation and/or
change in the proliferation of symbionts in different tissue layers.
Coral bleaching, the loss of symbiotic dinoflagellates (zooxanthellae) or their photosynthetic pigments in response to environmental stress, is of huge global concern. In contrast to tropical corals, which are highly sensitive to fluctuations in environmental parameters such as temperature, light and salinity, zooxanthellate invertebrates in temperate waters rarely bleach despite highly variable conditions. In this study, we tested the effects of salinity with combined effects of light and temperature stress on the photophysiology and stability of the temperate symbiotic sea anemone, Anthopleura aureoradiata, through chlorophyll fluorescence. In the field it was demonstrated that A. aureoradiata was resilient to abiotic fluctuations of considerable magnitude in the intertidal zone. Salinity was revealed to range naturally between a winter low of 30 and summer high of 40 ppt in an elevated tide pool with no measurable effects on the photophysiology of A. aureoradiata residing within. In a controlled environment, only extreme high and low salinities had an effect on the zooxanthellar photosystem, with a wide range of tolerance between 15-50 ppt dependent on the levels of temperature and light. Both high and low light, and temperature, also impacted upon photophysiology. Moreover, each of these variables independently, as well as combined, exacerbated the impact of salinity stress. In addition, the duration of exposure played an important role in the survival of this symbiosis, with only 48-96 h exposure to the extreme salinities of 5, 10, 55 and 60 ppt inducing irreversible photosynthetic failure, bleaching and death. Thus, the data supports the idea that this anemone-zooxanthellar symbiosis is highly resilient to considerable amounts of abiotic stress, a likely a function of the robust photophysiology of its zooxanthellae. This resilience to bleaching suggests that A. aureoradiata and its zooxanthallae have evolved a combination of powerful defensive mechanisms to help aid against the heterogenous environment from which they come. I will present an overview of these osmoregulatory mechanisms, photoacclimatory strategies and behaviours that this symbiosis likely deploys in order to combat environmentally realistic ranges in abiotic factors. Further studies would be necessary to deduce whether it is the host or zooxanthellae which are responsible for the breakdown of this symbiosis.
Reef-building scleractinian corals widely engage in symbiotic relationships with Symbiodinium dinoflagellates (zooxanthellae), which reside inside cells of the gastrodermis. In most cases, sexually produced larvae acquire their symbionts from the environment in the early developmental stages preceding settlement; however, some scleractinian corals maternally "seed" their oocytes with symbionts, and these symbionts are reported to be restricted to the gastrodermis at the time of its formation (gastrulation). A precise mechanism for how Symbiodinium are translocated to endoderm in these seeded species was previously unknown. In order to examine the process of endoderm formation and Symbiodinium localization during gastrulation, we have examined two species of "robust" clade scleractinians: Fungia scutaria (nonseeded) and Pocillopora meandrina (maternally seeded). We determined that both species, independent of whether or not they are seeded, undergo a "nutritive" stage before gastrulation, wherein lipid-rich cells (F. scutaria) or membrane-bound cellular fragments (P. meandrina) are passed to the blastocoel where they are subsequently taken up by the definitive endoderm. This emergent property of anthozoan development has been co-opted to facilitate the movement of Symbiodinium to the blastocoel (future site of endoderm), in the seeded species, where they are later phagocytosed by the newly formed definitive endoderm. Additionally, both species of robust clade scleractinians examined gastrulate by way of invagination, as do the majority of anthozoans. This invagination differs from the prawn chip-type gastrulation seen in the complex clade corals and provides evidence for a possible linkage between gastrulation type and phylogenetic history.
Little information is available on the sexual reproductive biology of anemones that provide essential habitat for anemonefish. Here we provide the first information on the surface ultrastructural and morphological changes during development of the embryos and planula larvae of Entacmaea quadricolor and Heteractis crispa, using light and scanning electron microscopy. Newly spawned eggs of E. quadricolor and H. crispa averaged 794 microm and 589 microm diameter, respectively, and were covered by many spires of microvilli that were evenly distributed over the egg surface, except for a single bare patch. Eggs of both species contained abundant zooxanthellae when spawned, indicating vertical transmission of symbionts. Fertilization was external, and the resulting embryos displayed superficial cleavage. As development continued, individual blastomeres became readily distinguishable and a round-to-ovoid blastula was formed, which flattened with further divisions. The edges of the blastula thickened, creating a concave-convex dish-shaped gastrula. The outer margins of the gastrula appeared to roll inward, leading to the formation of an oral pore and a ciliated planula larva. Larval motility and directional movement were first observed 36 h after spawning. E. quadricolor larval survival remained high during the first 4 d after spawning, then decreased rapidly.
The mode and tining of reproduc'tion, abundance and distribution were studied in four congeueric species of
hern"matypic coral on Heron Island reef, Great Barrier \*f.. Poites and.rewsi, P. lobota, P. lutea and P. ,nunayen'
sis have stable gonochorism with the former three species having a short annual period ofegg and sperm release,
fertilization being external, and the latter'having internd fertilization and an ertended larval release period. P.
andrcwsi, P. lafutc and P. luiea reproduce asexually when pieces &om large colonies are broken off and dispersed
by waves and currents. The abundance of the four species ol Paites on Heron Islend reef flat is rel,ated to tbe
relative success of sexual and aserual recruitment (fragrnentation).
Zooxanthellae in different stages of two opposite processes, degradation and proliferation, were found in the planulae of
hermatypic corals. The formation of new zooxanthellae is balanced by degraded zooxanthellae in newly released planulae. The
number of dividing zooxanthellae and degraded zooxanthellae during the day amounted to approximately 2 to 3% of the standing
stock. In settled planulae and particularly in motionless planulae of Stylophora pistillata (Esper, 1797), the degraded zooxanthellae outnumbered proliferous zooxanthellae. The proliferation and degradation of zooxanthellae
and the extrusion of degraded remnants of zooxanthellae are significantly phased. Swimming planulae are more autotrophic than
motionless planulae. The physiological parameters of settled planulae with exoskeleton are similar to those of adult polyps.
The significance of zooxanthella degradation in the vital functions of planulae is discussed. We suggest that the degradation
of zooxanthellae in planulae occurs by the digestion of symbionts by host cells.
The soft coral Anthelia glauca Lamarck, 1816, of the family Xeniidae, is found on the reefs of KwaZulu-Natal, South Africa. Its gastrodermal cells contain
numerous endosymbiotic unicellular algae (zooxanthellae). A. glauca is a gonochoric species that simultaneously broods its planulae within the pharyngeal cavity of the polyps. Symbiotic algae
appear with zygote formation within the pharynx, embedded in amorphous material. The algal cells adhere to the ciliated ectodermal
surface of immature planulae and are most probably endocytosed by them. Zooxanthellae are translocated towards the basal part
of the ectoderm. Gaps are subsequently opened in the mesoglea into which symbionts surrounded by ectodermally derived material,
including plasma membrane, pass. The basal membrane of endodermal cells disintegrates, and the algae bulge into spaces formed
in the underlying endoderm. Throughout the process, each zooxanthella resides within a vacuolar membrane in the detached ectodermal
cytoplasm. The acquisition process is essentially one in which zooxanthellae are translocated from the pharyngeal cavity into
the ectoderm and then through the mesoglea into the endoderm, culminating in the final symbiotic state. The direct transmission
of symbiotic algae to the eggs or larvae probably provides the most efficient means whereby zooxanthellae are acquired by
the host progeny.
The presence of zooxanthellae in tissues of the cold-temperate water coral Plesiastrea urvillei (Milne Edwards and Haime) has been confirmed histologically. Numbers of zooxanthellae per unit surface area and increases in submerged wet weight as a measure of calcification have been followed for 150 days under four different conditions: light-fed, light-starved, dark-fed, and dark-starved. No significant difference was found in density of zooxanthellae or calcification rates between light-fed and light-starved, and between dark-fed and dark-starved. After Day 48 the calcification rate in the dark dropped, however, by a factor of ≈4 to a constant lower rate and was correlated with a decrease in density of zooxanthellae. Zooxanthellae thus enhance calcification about 4 times during photosynthesis. Measurements of oxygen consumption and production indicated that even at the low light intensities experienced on a cloudy winter day by the coral in its natural environment more energy was fixed during photosynthesis than was required by the host. The retention of zooxanthellae and continued calcification in the dark for upwards of 48 days is considered to be an adaptation to the lower light levels experienced by P. urvillei compared with tropical corals.
Early embryogenesis of the internally brooding soft coral Xenia umbellata and acquisition of algal symbionts in the course of its planular ontogenesis have been examined by scanning and transmission electron microscopy and by light microscopy. The endoderm of adult X. umbellata harbours symbionts mainly in the tentacles and in the peripheral solenia system. The colonies are gonochoric brooders. Algal symbionts were never found in the sperm sacs, and were only rarely found in the follicular tissue enclosing the oocytes. Fertilized eggs pass into endodermal brood pouches where embryogenesis occurs. Cleavage is holoblastic and leads to formation of a solid blastula. Algal symbionts are conspicuously embedded in the parental mesoglea that coats the young embryo, most probably transmitted by surface adherence. At a further stage, this integument disappears and the algae reside extracellularly among the cells of the newly-formed blastula. After subsequent cell proliferation developing planulae possess an inner mass of yolk-laden cells that contain numerous symbiotic algae. Gradually the yolk disintegrates, leaving a cavity enclosed by ectoderm, a thin mesoglea and an inner endoderm with intracellular symbionts. The mature planulae have already been provided with numerous intracellular symbionts by the time they are expelled from the brood pouches. The markedly early symbiont acquisition by the embryos of X. umbellata may help support their developmental requirements in the course of planular ontogenesis.
Intracellular symbiotic dinoflagellates are associated with the tropical scyphozoan Linuche unguiculata (Swartz, 1788) throughout all stages of the host's life cycle. During sexual reproduction, eggs are released in mucus strands that contain symbiotic dinoflagellates. Fertilization and development take place externally in the water column. Epifluorescence and transmission electron microscopy showed that unfertilized eggs did not contain intracellular algae, but that infection of the developing embryo was generally successful by the 128-cell stage (10 h after fertilization at 23 C). However, experiments with artificially provided Cellufluor-labeled algae demonstrated that older embryos and planulae could be infected by algae through at least 24 h post-fertilization, indicating that the L. unguiculata symbiosis represents a semi-closed system. This novel mode of symbiont acquisition results in most sexually-produced offspring becoming infected with maternally-transmitted algae during early development, but allows for acquisition of non-maternally-provided algae later in development. Most of the algal symbionts during the early stages of embryonic and larval development are located within ectodermal cells. This is in contrast to the other life-cycle stages of L. unguiculata (i.e., scyphistoma, medusa, ephyra), where symbionts are found within the gastrodermis of the host.
The embryology of Anthopleura elegantissima and Anthopleura xanthogrammica is described. Ova of A. elegantissima are 120–150 μm in diameter and brown, while those of A. xanthogrammica are 175–225 μm in diameter and purple. In both species, cleavage is complete and equal: endoderm formation is by emboly. The planulae of both species are similar in appearance and are 150–250 μm in length with an apical tuft 60–75 μm in length. Feeding of the planulae is discussed, as is the function and phylogenetic significance of the apical sensory tuft of the planula.
The histological pathway by which intracellular symbiotic Chlorella move into the developing oocytes of hydra was investigated at the ultrastructural level. Algae move from within the digestive cells of the endoderm to within the oocytes of the ectoderm in a three-step process. First, the algae are released by digestive cells into the mesolamella (basement membrane). Second, the algae move as individual cells into the adjacent intercellular spaces of the ectoderm. Third, they are taken up by the oocyte by phagocytosis. This transfer occurs only in the central regions of the ovary, and only after oocytes have reached an advanced stage. Normally the mesolamella is separated from the ectodermal interstitial spaces by a layer of epitheliomuscular cell muscle processes. This layer degenerates in the region where algae will move into the ectoderm. This study shows that algae move as individual cells and not intracellularly within processes of the epithelial cells.
On the Red Sea coral reefs Litophyton arboreum is a common octocoral whose endodermal cells are associated with endosymbiotic dinoflagellates (zooxanthellae). Colonies of this species are gonochoric and brood planulae which, upon release, are already associated with the algal symbionts. Algal cells within membrane-bound vacuoles are observed within the gastrovascular cavity of the polyps, adjacent to the oocytes and are gradually phagocytized by the follicular cells which surround the oocytes. During oogenesis, temporary gaps open in the mesoglea underlying the follicular cells. Symbionts within vacuoles, along with cytoplasm and various organelles derived from the follicular cells, are translocated through these gaps. Subsequently, groups of zooxanthellae accumulate at the perioocytic zone, flanked between the mesoglea and oocytic microvilli. At a later stage, prior to the commencement of the breeding season, symbionts pass through the oolemma and rest inside the periphery of the oocytes. It is proposed that early uptake of zooxanthellae by sexual progeny at the oocyte stage, indicates a highly specialized mode of interaction between this algal symbiont and its host.