Expulsion of zooxanthellae by symbiotic cnidarians from the Red Sea

The expulsion of zooxanthellae by octocorals (Xenia macrospiculata and Heteroxenia fuscescens), the scleractinian coral Stylophora pistillata, and the hydrocoral Millepora dichotoma, was measured in the field. The numbers expelled did not exceed 0.1% of the total standing stock of symbiotic algae per day, the rate of expulsion was less than 4% of the rate at which cells are added to symbiotic populations, and the carbon lost represented 0.01% of the total carbon fixed on a daily basis. Expulsion of zooxanthellae is therefore not a significant sink for fixed carbon in these symbiotic associations. In contrast to field populations, expulsion by X. macrospiculata increased 5-fold or more in the laboratory, suggesting that laboratory conditions may introduce stress.     

Substratum preferences and planulae settling of two red sea alcyonaceans: Xenia macrospiculata Gohar and Parerythropodium fulvum fulvum (Forskl)

The settling behaviour and substratum preferences of the planulae of the Red Sea soft corals Xenia macrospiculata Gohar and Parerythropodium fulvum fulvum (Forskl) were examined in the laboratory. The planulae of the two species have a short pelagic phase and they tend to settle immediately upon leaving the parent colonies. Mucous secretion is used by the larvae for crawling and adhering to the substratum. They exhibit an aggregated pattern of settlement. The developing polyps are found in depressions or pits of the substratum. The planulae preferentially settle on rough substrata and avoid smooth surfaces. They search for substrata covered with an organic coating, composed of turf or crustose coralline algae. Such substrata create better conditions for larval settlement and metamorphosis. The planulae of P. f. fulvum exhibit a striking preference for upside-down attachment on undersides of the substrata, while Xenia macrospiculata utilizes both substratum faces for settlement. Light intensity seems insignificant in determining attachment sites. The findings of the experiments correspond well with the distributional patterns of juveniles of the two species as found in the natural environment. The specific requirements for settling of both species increase their chances of successful development and thus enhance their survival.     

Size variation of planulae and its effect on the lifetime of planulae in three pocilloporid corals

Dispersal of propagules plays an important role in the distribution of corals. Pocillopora damicornis, Seriatopora hystrix, and Stylophora pistillata are all brooders and release planulae having symbiotic zooxanthellae. Planulae showed a great size variation, especially at peaks of planulation, and we found negative correlations between zooxanthella density and planula size in S. hystrix and S. pistillata. Studies of the larval life of planulae under both light and dark conditions have revealed that larger planulae have a longer lifetime. When planulae of the same size were compared, it was found that they lived longer under light conditions than under dark conditions. These findings suggest that planulae utilize energy from photosynthetic products of zooxanthellae and that these corals enjoy long-distance dispersal by producing larger planulae with greater dispersal potential. It is conceivable that variation in the dispersal potential of planulae is a means of adaptation by which planulae can increase their chances of finding a suitable habitat.     

Lipid content of Favia fragum larvae: changes during planulation

Lipid content of planula larvae of the brooding scleractinian coral Favia fragum was analysed through a monthly planulation period. The average lipid content per dry weight of F. fragum planulae was 39%, which is low compared with other scleractinian coral species. Lipid content of planulae was significantly affected by the day of release and decreased during the planulation period.     

Feeding increases the number of offspring but decreases parental investment of Red Sea coral Stylophora pistillata

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Reef waters stimulate substratum exploration in planulae from brooding Caribbean corals

This study tested the hypothesis that waters surrounding reefs with healthy coral populations are more likely than degraded sites to induce planulae to navigate downward and begin benthic probing. In the laboratory, larvae from two brooding Caribbean coral species, Agaricia tenuifolia and Porites astreoides, were introduced to seawater collected at (1) 1 m above shallow, healthy reef with high-coral cover, (2) 1 m above shallow, degraded reef with high-macroalgal cover, and (3) ~400 m ocean-ward of the reef in deep, blue water. Counter to the hypothesis, water from both the healthy and degraded reef caused the larvae to swim downward and begin benthic probing. These results suggest that substances carried in reef waters may contribute to macro-scale habitat selection by planulae and that understanding how these waterborne cues mesh with other stimuli used by planulae to select a settlement site may be valuable for deciphering a site’s recruitment potential for corals.     

Larval development and survivorship in the corals Favia favus and Platygyra lamellina

Two Red Sea faviid species, Favia favus and Platygyra lamellina spawn eggs and sperm once a year, during the summer. External fertilization occurs 0.5 h after spawning, and mobile gastrulae appear 20 h later. Four stages in the early ontogenesis of these corals are described. The slow development (2–3 months) to the polyp stage in broadcasting species is attributed to the lack of zooxanthellae in their planulae and their appearance in the primary polyp only at a later stage. Survivorship of one-month-old primary polyps is ca 0.21% and 0.25% in F. favus and P. lamellina respectively, from the populations of 2–9-day-old planulae. Despite these low rates of survival, both species form dense populations in the Gulf of Eilat.     

Metamorphosis and acquisition of symbiotic algae in planula larvae and primary polyps of Acropora spp.

Coral planulae settle, then metamorphose and form polyps. This study examined the morphological process of metamorphosis from planulae into primary polyps in the scleractinian corals Acropora nobilis and Acropora microphthalma, using the cnidarian neuropeptide Hym-248. These two species release eggs that do not contain Symbiodinium. The mode of acquisition of freshly isolated Symbiodinium (zooxanthellae) (FIZ) by the non-symbiotic polyp was also examined. Non-Hym-248 treated swimming Acropora planulae did not develop blastopore, mesenteries or coelenteron until the induction of metamorphosis 16 days after fertilization. The oral pore was formed by invagination of the epidermal layer after formation of the coelenteron in metamorphosing polyps. At 3 days after settlement and metamorphosis, primary polyps exposed to FIZ established symbioses with the Symbiodinium. Two–four days after exposure to FIZ, the distribution of Symbiodinium was limited to the gastrodermis of the pharynx and basal part of the polyps. Eight–ten days after exposure to FIZ, Symbiodinium were present in gastrodermal cells throughout the polyps.     

Early development of zooxanthella-containing eggs of the corals Porites cylindrica and Montipora digitata: The endodermal localization of zooxanthellae

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.     

Seasonality and lunar periodicity in the reproduction of Pocilloporid corals

Reproductive seasonality and lunar periodicity of planula release were investigated for the three brooding coralsPocillopora damicornis, Seriatopora hystrix, andStylophora pistillata at Heron Island in the southern Great Barrier Reef. Branch fragments collected from undisturbed colonies in the field were used to determine when planulae were present for all three species, and direct observations of planula release were made on colonies ofPocillopora kept in aquaria. All three species displayed marked seasonal variation in reproductive output, with nearly all reproductive activity occurring over the summer months.Pocillopora exhibited distinct lunar periodicity in planulation, with planula release occurring around three quarter moon, and no planulae being present in samples collected between new and full moons.Seriatopora also displayed lunar periodicity of planula release, although it was not as distinct as forPocillopora, whileStylophora did not show any lunar periodicity.     

Sexual reproduction and larval settlement of the zooxanthellate coral Alveopora japonica Eguchi at high latitudes

Sexual reproduction and larval settlement of Alveopora japonica Eguchi were studied at its northernmost distribution in Tokyo Bay (34°58'03'N, 139°46'05'E), where the annual sea temperature ranges from 13 to 27 °C. Alveopora japonica is a hermaphroditic brooding coral with oocytes and spermaries developing on separate mesenteries of the polyp. The oocytes first appeared in October, maturing in late August to early September of the following year, whereas the spermaries were first observed in May, and matured in approximately 4 months. The oocytes reached ca. 800 µm in diameter. Planulae containing zooxanthellae in their endoderm were released during the daytime in September and October. Well-developed planulae were able to settle and metamorphose within 7 h. The polyps started budding about 3 weeks after settlement, and took 3 years to grow to maturity. The population examined was sexually reproductive, indicating that A. japonica maintains local populations in Tokyo Bay by sexual reproduction.     

Highly stable symbioses among western Atlantic brooding corals

The reproductive mode of corals largely determines how zooxanthellae (Symbiodinium spp.) are acquired. Typically, broadcast spawning corals obtain symbionts from the surrounding environment, whereas most brooders transfer symbionts from maternal parent to offspring. Brooding corals are therefore predicted to harbor stable communities of Symbiodinium. This study documents the associations between Symbiodinium spp. and brooding corals in response to seasonal environmental fluctuations. Between March 2002 and December 2005, endosymbiont identity was determined seasonally from replicate colonies (n = 6) of three brooding species, Agaricia agaricites, Porites astreoides and Siderastrea radians, from shallow environments (1–4 m) of the Florida Keys and Bahamas. Symbionts were identified via denaturing gradient gel electrophoresis (DGGE) of the internal transcribed spacer 2 (ITS2) region. No change was detected in the Symbiodinium communities harbored within these brooding colonies. Additionally, no change in symbiosis was observed through a moderate bleaching event, thereby demonstrating that some bleached corals recover without changing symbionts.     

Kalisomes in corals: a novel KCl concentrating organelle?

Large membrane-bound inclusions were clearly visible within the gastrodermis and lipid-containing cells of planulae and settled larvae of the zooxanthellate coral, Pocillopora damicornis after fixation or freeze-substitution. We suggest that these inclusions may be a novel potassium (kalium) chloride concentrating organelle, for which we propose the name kalisome. The inclusions were more abundant in settled larvae than in planulae and were not present in mature polyps. In planulae of the azooxanthellate coral, Dendrophyllia sp. these inclusions were extremely rare. Quantitative X-ray microanalysis of freeze-substituted preparations showed that the inclusions in P. damicornis settled larvae contained very high, positively correlated, concentrations of K (2.5 mol x kg(-1)) and Cl (2.5 mol x kg(-1)). Lower concentrations of both K (1.2 mol x kg(-1)) and Cl (1.3 mol x kg(-1)) were detected in P. damicornis planulae, yet higher concentrations were measured in Dendrophyllia planulae (K=6.0 mol x kg(-1); Cl=5.1 mol x kg(-1)). No significant (P>0.05) differences in concentration were observed between inclusions in freeze-substituted and freeze-dried sections of planulae. Symbiotic algae (zooxanthellae) in P. damicornis planulae and settled larvae also contained deposits with high levels of K and Cl, but these were not positively correlated and no structures associated with them were retained by fixation. Significant (P<0.05) concentration differences were also observed between deposits in freeze-substituted and freeze-dried sections. However, similar to 'kalisomes,' zooxanthellae deposits were more abundant in settled larvae than planulae and absent in mature polyps. Higher concentrations of K and Cl were also detected in settled larvae (K=0.7 mol x kg(-1); Cl=1.1 mol x kg(-1)) in comparison to planulae (K=0.4 mol x kg(-1); Cl=0.5 mol x kg(-1)).     

Early development and acquisition of Zooxanthellae in the temperate symbiotic sea anemone Anthopleura ballii (Cocks)

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.     

Linking micromorphism,brooding, and hermaphroditism in brachiopods: Insights from Caribbean Argyrotheca (Brachiopoda)

In extant brachiopods, parental brooding of the larvae occurs exclusively within Rhynchonelliformea. Methods of larval protection range from simple retention of the larvae within the mantle cavity, to sophisticated brood care within highly specialized brood pouches found in Argyrotheca and Joania (Terebratulida, Megathyridoidea), Gwynia (Terebratulida, Gwynioidea), and all Thecideoidea (Thecideida). Previous studies on the reproductive biology of Argyrotheca yielded contrasting results on the epithelial origin of the brood pouches in this genus. Here, representatives of different species of Argyrotheca from the Belize Barrier Reef were examined using histological section series. Brood pouches of four species, A. cf. schrammi and Argyrotheca sp. 1–3, are of the same basic structure, formed by invaginations of the anterior body wall and connected to the visceral cavity via the metanephridia. The same four species are simultaneously hermaphroditic, suggesting that fertilization is achieved, at least partly, through selfing. One species, Argyrotheca rubrocostata, differs significantly from all others as it has no brood pouch and gonochoric gonads. Thus, the presence of brood pouches and simultaneous hermaphroditism are concluded to be correlated within Megathyridoidea and proposed to be homologous traits of Joania and several but not all species of Argyrotheca, questioning the monophyletic status of both genera. In contrast to the brood pouches of Thecideoidea, lophophoral epithelium is not involved in the formation of the pouches of Argyrotheca and Joania. Therefore, megathyridoid and thecideoid brood pouches are not homologous but evolved independently within rhynchonelliform brachiopods. All brachiopods with brood pouches share a micromorphic form and a short life span, limiting the space and time available for gamete and larval development. We suggest that the brood pouches and the hermaphroditic gonads of Argyrotheca spp. and Joania compensate these limitations by minimizing the loss of gametes and larvae, and by maximizing the chances of successful fertilization. J. Morphol., 2013. © 2013 Wiley Periodicals, Inc.     

Reproduction and developmental pathways of Red Sea Xeniidae (Octocorallia,Alcyonacea)

This work on Red Sea alcyonaceans describes the reproductive patterns of 21 xeniid species. Gonochorism is the commonest sexual mode but simultaneous hermaphroditism was recorded in 4 species and brooding of planulae was observed in 15 species. The reproductive patterns of Xenia umbellata and Heteroxenia fuscescens were examined. X. umbellata exhibits seasonal spermatogenesis, continuous oogenesis and a 7 month period of planulation each year. H. fuscescens has continuous gametogenesis, and planulation occurs throughout the year, lacking any lunar pattern. The prolonged breeding season of H. fuscescens reflects intrapopulation asynchrony in larval development and subsequent maturation. Xeniids possess structurally similar gonads, but adopt diverse reproductive and developmental pathways.     

Fish assemblage structure in urban streams of Puerto Rico: the importance of reach- and catchment-scale abiotic factors

Cotylorhiza tuberculata is a common symbiotic scyphozoan in the Mediterranean Sea. The medusae occur in extremely high abundances in enclosed coastal areas in the Mediterranean Sea. Previous laboratory experiments identified thermal control on its early life stages as the driver of medusa blooms. In the present study, new ecological aspects were tested in laboratory experiments that support the pelagic population success of this zooxanthellate jellyfish. We hypothesized that planulae larvae would have no settlement preference among substrates and that temperature would affect ephyra development, ingestion rates and daily ration. The polyp budding rate and the onset of symbiosis with zooxanthellae also were investigated. Transmission electron microscopy revealed that zooxanthella infection occurred by the polyp stage. Our results showing no substrate selectivity by planulae and high polyp budding rates in high temperatures suggest increased benthic polyp populations, which would lead to higher medusa abundances. Rates of transition from ephyrae to medusae and the feeding of early medusa stages also increased with temperature. Continuing changes in coastal ecosystems such as future climate warming and marine construction may lead to increased populations of jellyfish to the detriment of fish globally.     

Reproductive biology of the Caribbean brooding octocoral Antillogorgia hystrix

The reproductive biology of the Caribbean gorgonian Antillogorgia hystrix was studied in the shallow‐water reefs of Cross Harbour, Great Abaco (The Bahamas) from 2009 to 2010. Antillogorgia hystrix is an internal brooder that reproduces annually. The population at Cross Harbour was gonochoric and the sex ratio was skewed toward females (~3:1). Oogenesis precedes spermatogenesis by several months, and lasts at least 9 months, with oocytes >100 μm in diameter first becoming visible in dissections of samples from February; mature oocytes are present in late October–November. The size of mature oocytes (400–900 μm in diameter) was greater than that of the spermaries, which were rarely larger than 400 μm. Brooded planulae were observed in polyps from early November to mid‐December, and planula release was observed in aquaria in December 2009, which suggests that planulation occurs continuously over this period. Planulae of A. hystrix contained dinoflagellate symbionts, presumably acquired during embryogenesis and/or by mature planulae while they were in the gastrovascular cavity of the polyp. Brooding is an uncommon reproductive strategy among Caribbean gorgonians and this is the first report of internal brooding in the genus Antillogorgia. The genus contains a number of sympatric species with different modes of reproduction, and knowledge of their reproductive biology is critical to understand their ecology and evolution.