Reproduction in Anthelia glauca (Octocorallia: Xeniidae). II. Transmission of algal symbionts during planular brooding

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. Received: 15 July 1997 / Accepted: 25 February 1998     

Strobilation,budding and initiation of scyphistoma morphogenesis in the rhizostome Cassiopea andromeda (Cnidaria: Scyphozoa)

Scyphistomae of Cassiopea andromeda Forskål, 1775 containing symbiontic zooxanthellae did not develop medusae at a constant temperature of 20°C, but monodisc strobilation was initiated after transfer of the polyps to 24°C. After release of the ephyrae and regeneration of the hypostome and tentacular region, the recovered polyps either produced vegetative buds or entered a new strobilation phase. Formation of motile, planula-like buds was not found to be indicative of unfavourable environmental conditions. Intensity of budding was positively correlated with available food and with increase of temperature. Budding was negatively correlated with the number of polyps maintained per dish and with the conditioning of the sea water. Under optimal feeding and temperature conditions, polyps could simultaneously produce chains of buds at 2 to 4 budding regions. Settlement and development of buds into scyphistomae was suppressed in pasteurized sea water and in pasteurized sea water containing antibiotics, but polyps developed from buds in the presence of algal material taken from the aquarium, debris or egg shells of Artemia salina, or on glass slides which had been incubated in used A. salina culture medium. Several species of marine bacteria were detected after staining these slides. One, a Gramnegative coccoid rod, which was identified as a nonpathogenic Vibrio species, was isolated, cultivated as a pure strain, and was proved to induce the development of C. andromeda buds into polyps. Millipore filter-plates coated with Vibrio sp. cells grown in suspension culture were ineffectual, but diluted filtrate initiated polyp morphogenesis. The inducing factor is obviously not a constituent of the bacterial cell surface, but is a product of growing Vibrio sp. cells released into the medium. This product was found to be relatively heat-stable and dialyzable. As to the basic mechanism involved in the induction of polyp formation, it is suggested that the inducing factor (s) acts bimodally by inducing pedal disc development and by eliminating a head inhibitor originating from the basal end of the bud. The life history, and various aspects of medusa-formation and of vegetative reproduction in scyphozoans are reviewed and discussed with particular reference to rhizostome species. Special attention has been paid to some reports of larval metamorphosis controlled by marine bacteria.     

In vivo binding of a biologically active oligopeptide in vegetative buds of the scyphozoan Cassiopea andromeda: demonstration of receptor-mediated induction of metamorphosis

Vegetative buds of Cassiopea andromeda (Cnidaria, Scyphozoa) metamorphose into polyps in the presence of short synthetic peptides containing proline as the preterminal amino acid at the carboxyl terminus. In an in vivo assay, the binding of the biologically active hexapeptide ¹⁴C-dansyl-GPGGPA in buds was shown to be specific and saturable. Scatchard plot analysis of the specific binding data revealed a dissociation constant (K _D) of about 7 M. The total number of receptors was calculated to be approximately 1×10¹⁰ bud^-1 under saturation conditions. In correlation with the results of prior investigations, our finding of receptor-mediated induction of metamorphosis strongly supports the hypothesis that binding of biologically active peptides to receptors leads to initiation of phosphatidylinositol breakdown and activation of protein kinase C.     

Embryogenesis and acquisition of algal symbionts by planulae of Xenia umbellata (Octocorallia: Alcyonacea)

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.     

Morphological and functional development of larval and juvenile Limanda yokohamae (Pisces: Pleuronectidae) reared in the laboratory

Morphological and behavioural aspects in larval development need to be studied in detail to understand the early life history better, and to gain a comprehensive knowledge on early life stages for fish species important in aquaculture and fisheries. In the present study, larvae of Limanda yokohamae (Günther) were reared to observe their behavioural development, and to obtain specimens for studying the morphological features and the intestinal development at Ohno, Hiroshima, Japan, in 1987. Swimming activity was monitored at several larval stages, and swimming speed was recorded until settlement and after-feeding behaviour was initiated. A slight increment of swimming speed was observed with larval growth. Larvae changed their swimming behaviour from surface waters to the bottom of the rearing tank when their eyes began to move. Morphological development of pigmentation patterns, fin development, squamation and the development of the digestive tract were described and illustrated in detail to characterize development stages, especially those relating to metamorphosis. During metamorphosis, growth ceased and rapid changes in allometric growth were accompanied by differentiation of the digestive tract. After metamorphosis there was steady growth, allometric growth achieved a constant value, and both the scales and digestive organs were fully formed. Metamorphosis was therefore a crucial developmental milestone, including a critical phase during which survival potential was lowered.     

Comparison of telomere length among different life cycle stages of the jellyfish Cassiopea andromeda

The polyp (scyphistoma) of the jellyfish Cassiopea andromeda reproduces asexually repeatedly, while the medusa, the sexually reproducing stage, exhibits a relatively shorter life span. As a first step to understand the mechanism behind the differences in the life spans of the polyp and medusa stages of the jellyfish, we compared the lengths of the telomere region of one targeted chromosome between the polyp and medusa stages using a modified single telomere length assay (STELA). The double-stranded regions of the telomeres were amplified by PCR, and the average length of the PCR products was estimated by densitometry analysis of the gel smear. Chromosomes within cells of the bell region of the medusa were characterized by longer telomeres than those of polyps, asexual propagules, or other regions of the medusa. This is the first study to estimate the telomere lengths of targeted chromosomes in a cnidarian and opens a way to understand the mechanism underlying different life spans of the polyp and medusa stages.     

Requirement of exogenous inducers for metamorphosis of axenic larvae and buds of Cassiopea andromeda (Cnidaria: Scyphozoa)

Planula larvae and asexually-produced buds of the rhizostome scyphozoan Cassiopea andromeda (collected throughout the year in Eilat, Israel) have the ability, under axenic conditions, to attach to a substrate and undergo morphogenetic development to form a polyp (=scyphistoma) in: (1) the presence of unidentified inducers found in the adult habitat and (2) the presence of cefined organic compounds. Axenic planulae and buds were unable to settle and complete metamorphosis in autoclaved artificial or natural seawater from the North Sea when maintained without food, but continued swimming while decreasing in size and protein content, eventually dying within three months. When maintained in autoclaved seawater from the Red Sea, between 25 and 46% of the planulae and 4 and 11% of the buds metamorphosed within 30 d. Axenic solutions of cholera toxin, thyroid stimulating hormone, and pancreatic casein hydrolysate peptides in artificial seawater induced morphogenic development of 20 to 100% of planulae and buds within 2 to 18 d. The natural inducer(s) in Red Sea seawater, though unidentified, may have characteristics similar to the large proteins and small peptide inducers used in this study. Planulae and buds older than 20 d metamorphosed sooner and responded to lower concentrations of pancreatic casein hydrolysate peptides than younger individuals. This may be a physiological mechanism for enhancing metamorphosis and survival in nature. The data show that settlement and metamorphosis can be induced by solutions of cholera toxin and thyroid stimulating hormone, suggesting that, as in mammalian systems, the mechanism of action of these chemicals may involve cyclic adenosine monophosphate (cAMP) as an intermediate messenger. However, dibutyric cAMP, which is capable of passing through membranes and functioning normally inside the cell, did not induce metamorphosis of buds, and the levels of intracellular cAMP in buds and larvae typically increased slowly during induction of metamorphosis, unlike the high and rapid increases associated with cAMP-mediated biochemical events in mammalian cells. These results suggest that the observed cAMP changes seen were associated with metamorphic development, but not with the triggering mechanism.     

Availability of dissolved organic matter offsets metabolic costs of a protracted larval period for <Emphasis Type="Italic">Bugula neritina</Emphasis> (Bryozoa)

For nearly a century researchers have investigated the uptake and utilization of dissolved organic matter (DOM) by marine invertebrates, but its contribution to their growth, reproduction, and survival remains unclear. Here, the benefit of DOM uptake was assessed for the marine bryozoan Bugula neritina (Linnaeus 1758) through performance comparisons of individuals in the presence and absence of DOM. The experiments were performed using B. neritina collected from floating docks in Beaufort, NC, USA from July to September 2004. Seawater was subjected to ultraviolet irradiation to reduce naturally occurring DOM, and then enriched with either 1 μM of palmitic acid or a mixture containing 1 μM each of glucose, alanine, aspartic acid and glycine. Larvae in DOM-enriched and DOM-reduced treatments were sampled and induced to metamorphose following 1, 6, 12, and 24 h of continuous swimming at 25°C. Sampled larvae were assessed for initiation of metamorphosis, completion of metamorphosis, and ancestrular lophophore size to determine the extent to which energy acquired from DOM uptake could offset the metabolic costs of prolonged larval swimming. DOM treatment had no significant effect on initiation of metamorphosis, but did have a significant effect on completion of metamorphosis and lophophore size. Larvae swimming in DOM-enriched treatments for 24 h experienced a 20% increase in metamorphic completion rate, compared to larvae swimming for 24 h in the DOM-reduced treatment. In addition, larvae in the amino acid and sugar mixture for 24 h had a significantly larger lophophore surface area and volume (23 and 31%, respectively), compared to larvae in DOM-depleted seawater. To ensure that the increases in performance found in larvae with access to DOM were not due to a decrease in metabolic activity, the respiration rates for these larvae were compared to those of larvae in DOM-depleted seawater. There were no significant differences between these treatments, indicating that the increases in performance were due to the energy acquired from DOM. These results clearly show that for B. neritina, DOM uptake results in increased metamorphic success and in the size of the feeding apparatus following an extended larval swimming duration.     

Asexual reproduction in homoscleromorph sponges (Porifera; Homoscleromorpha)

Asexual reproduction by external budding in Homoscleromorpha is reported for the first time. Two Mediterranean sponge species were studied, Oscarella lobularis and O. tuberculata. Buds are formed in the marginal basal part of sponge. Budding takes from 1 to 4 days and is defined in three budding stages. First, small irregular protuberances, consisting of external parental tissue, are formed. Second, they elongate and acquire more regular, nipple-like shape. These protuberances are tube like, their internal cavity derived from parental exhalant canal. The wall consists of three layers: (a) external layer is flagellated exopinacoderm, (b) internal one is flagellated endopinacoderm and (c) intermediate one is a thin layer of mesohyl. Third, a spherical bud with a large central cavity is formed. During budding, we did not observe cell proliferation or transdifferentiation either in budding zone or in any special mitotically active region. The bud attached to the substrate is similar to the rhagon developing after larva metamorphosis, it has a syconoid organization. Morphogenetically, budding in Oscarella differes from that in other sponges. Occurring by epithelial morphogenesis, it is similar to morphallaxis during regeneration. The presence in Homoscleromorpha of an epithelial morphogenesis is unique among sponges. This feature is shared by Homoscleromorpha and Eumetazoa.     

Dissolved histamine: a potential habitat marker promoting settlement and metamorphosis in sea urchin larvae

Many species of marine invertebrate larvae settle and metamorphose in response to chemicals produced by organisms associated with the adult habitat, and histamine is a cue for larvae of the sea urchin Holopneustes purpurascens. This study investigated the effect of histamine on larval metamorphosis of six sea urchin species. Histamine induced metamorphosis in larvae of three lecithotrophic species (H. purpurascens, Holopneustes inflatus and Heliocidaris erythrogramma) and in one planktotrophic species (Centrostephanus rodgersii). Direct comparisons of metamorphic rates of lecithotrophic and planktotrophic larvae in assays cannot be made due to different proportions of larvae being competent. Histamine (10 μM) induced metamorphosis in 95% of larvae of H. purpurascens and H. inflatus after 1 h, while the coralline alga Amphiroa anceps induced metamorphosis in 40–50% of these larvae. Histamine (10 μM) and A. anceps induced 40 and 80% metamorphosis, respectively, in the larvae of H. erythrogramma after 24 h. Histamine (10 μM) and the coralline alga Corallina sp. induced 30 and 70% metamorphosis, respectively, in the larvae of C. rodgersii after 24 h. No metamorphosis of any larval species occurred in seawater controls. Larvae of two planktotrophic species (Tripneustes gratilla and Heliocidaris tuberculata) did not metamorphose in response to histamine. Seagrasses, the host plants of H. inflatus, induced rapid metamorphosis in larvae of the two Holopneustes species, and several algae induced metamorphosis in C. rodgersii larvae. Histamine leaching from algae and seagrasses may act as a habitat marker and metamorphic cue for larvae of several ecologically important sea urchin species.     

Growth and differentiation during delayed metamorphosis of feeding gastropod larvae: signatures of ancestry and innovation

Extent of larval growth among marine invertebrates has potentially profound implications for performance by benthic recruits because body size influences many biological processes. Among gastropods, feeding larvae often attain larger size at metamorphic competence than non-feeding larvae of basal gastropod clades. Delay of metamorphosis can further influence size at recruitment if larvae continue to grow during the delay. Some caenogastopod larvae grow during delayed metamorphosis, but opisthobranch larvae do not. Data on larval growth of neritimorph gastropods are needed to help determine which of these growth patterns for planktotrophic gastropod larvae is more derived. We cultured planktotrophic larvae from all three major gastropod clades with feeding larvae through delays of metamorphosis of 3–10 weeks. Larvae of the caenogastropod Euspira lewisii and the euthyneurans Haminoea vesicula (Opisthobranchia) and Siphonaria denticulata (Pulmonata) conformed to previously described growth patterns for their respective major clades. Furthermore, the caenogastropod continued to lengthen the prototroch (ciliary band for swimming and feeding) and to differentiate prospective post-metamorphic structures (gill filaments and radular teeth) during delayed metamorphosis. Larvae of the neritimorph Nerita atramentosa arrested shell growth during delayed metamorphosis but the radula continued to elongate, a pattern most similar to that of non-feeding larvae of Haliotis, a vetigastropod genus. Character mapping on a phylogenetic hypothesis suggests that large larval size and capacity for continued growth during delayed metamorphosis, as exhibited by some caenogastropods, is a derived innovation among feeding gastropod larvae. This novelty may have facilitated post-metamorphic evolution of predatory feeding using a long proboscis.     

An energy budget for the free-swimming and metamorphosing larvae of Balanus balanoides (Crustacea: Cirripedia)

Analysis of biochemical components and measurements of oxygen consumption rates of cypris larvae of Balanus balanoides (L.) maintained in the laboratory at 10°C for up to 5 weeks after capture shows that lipid is the primary energy reserve, although later protein is utilised. Initially, the cyprids swim freely with an oxygen consumption rate of ca. 37×10^-3 l O₂ h^-1 cyprid^-1, but within a few days the rate falls to ca. 21×10^-3 l O₂ h^-1 cyprid^-1 when they cease swimming and explore the substratum. The cost of metamorphosis was calculated both from the loss of biochemical components and oxygen consumption rates during metamorphosis; the values were 2.8×10^-2 and 3.2×10^-2 cal cyprid^-1, respectively. A budget was collated from the data on respiration and biochemical composition, whereby the energy per cyprid was partitioned into that required for essential structural components (6.8×10^-2 cal), that needed for metamorphosis (3.0×10^-2 cal) and an excess available for swimming and exploring, which in the batches studied was about 5.0×10^-2 cal. This excess is mainly derived from the utilisation of lipid reserves and is used up usually 2 1/2 to 4 weeks after capture. During these measurements, samples of cyprids were taken at weekly intervals to test the rate of settlement and success of metamorphosis. The results showed that they lose their competence to metamorphose successfully approximately at the same time (3 to 4 weeks) that the energy supply for swimming and exploration is used up.     

Some observations on gametogenesis,larval development and substratum selection of the sea pen Ptilosarcus guerneyi

Ptilosarcus (Leioptilus) guerneyi (Gray) maintained in the laboratory, were observed to spawn in late March, 1972. Gametes, developed in the leaf proper, discharged through the mouths of feeding polyps and were fertilized externally in the sea water. The sea pen's eggs are 500 to 600 in diameter; a large female is capable of producing over 200,000 eggs in one season. A pear-shaped and free-swimming planula larva developed 4 days after fertilization, at a temperature of 12 °C. The larvae were ready to settle and metamorphose when 7 days old if favorable substratum was available, but would remain as planulae for at least 30 days if kept in glass dishes only. The 30-day-old larvae would metamorphose if a suitable substratum (coarse sand, for example) was presented. The larvae do not feed and, hence, development is lecithotrophic. Studies of histogenesis showed that metamorphosis greatly enhanced the rate of cellular differentiation. The high fecundity, lecithotrophic development, and the ability of substratum selection by the larvae explain the success of this species in maintaining a high-density population in many areas of sandy substratum in the shallow waters of Puget Sound (USA), despite the fact that it is preyed upon by 7 species of predators.     

Permeability of the oral epithelial layers in cnidarians

In order to characterize the permeability of the oral epithelial layers in cnidarians, we investigated the kinetics of transport of labelled ions (⁴⁵Ca,²²Na,³⁶Cl) and organic molecules (¹⁴C-inulin-carboxyl,¹⁴C-ala) through the oral tissue of two cnidarian species,Anemonia viridis (Forsskål, 1775) andHeliofungia actiniformis (Quoy and Gaimard, 1833) using the Ussing chamber method. In both species, unidirectional Ca, Na and Cl fluxes were the same in both directions (ectoderm towards endoderm and vice versa), the net flux being equal to zero. The insensitivity of these unidirectional transepithelial fluxes to metabolic inhibitor (1 mM sodium cyanide) and calcium channel inhibitor (100 M verapamil) and their linear dependence on calcium concentration suggest that these fluxes are simple driven by diffusion via a paracellular pathway. The epithelial layers were not permeable to inulin. Low-molecular weight amino acids such as alanine did not cross the epithelia but were absorbed by the ectoderm. The permeability coefficients indicate that the oral epithelial layers are leaky. It is suggested that the coelenteric cavity represents a compartment in which the ionic pool can be entirely renewed by simple diffusion. This process seems efficient enough to meet all calcium requirements in scleractinian corals.     

Competence and delay of metamorphosis in the Pacific oysterCrassostrea gigas

The temporal relationship between the onset of behavioral and morphogenetic competence was determined inCrassostrea gigas (Thunberg) larvae by exposure to appropriate chemical inducers during development. Larvae exhibited settlement behavior in response to L-3,4-dihydroxyphenylalanine (L-DOPA) before becoming competent to metamorphose in response to epinephrine. For larvae past the onset of competence, the apparent stimulus-threshold decreased and they were increasingly likely to metamorphose subsequent to induced settlement behavior. In the absence of chemical stimulation, cultured oyster larvae were able to delay metamorphosisand maintain competence for at least 30 d. Competence was correlated with, but not dependent upon, larval size and eyespot development. A mechanistic model of oyster settlement and metamorphosis is proposed which incorporates these new data.Contribution # 136 from the Center of Biotechnology, Marine Biotechnology Institute, University of Maryland     

Tale of two colors: <Emphasis Type="Italic">Cladopsammia gracilis</Emphasis> (Dendrophylliidae) color morphs distinguished also by their genetics and ecology

Cladopsammia gracilis (Dendrophylliidae), an ahermatypic coral inhabits the northern Red Sea. Two color morphs (pink and orange) are found aggregated in caves devoid of hermatypic corals, associated with crustose coralline algae (CCA). Sequencing the rDNA ITS region revealed a separate clustering of members of each color morph. Both morphs grow in shallow waters, with orange corals limited to the upper 4 m, while some pink coral aggregates thrive deeper than 30 m. Planulae were released between June and December. Pink planulae treated with antibiotics and exposed at different intervals to CCA, were competent and metamorphosed even 110 days after release. Maximal competency period for orange planulae was 70 days. All planulae were enhanced to metamorphose in presence of CCA. The mean age at metamorphosis of pink and orange planulae treated with CCA differed significantly. Most orange planulae settled directly on the CCA while most pink planulae settled on the wall of the experiment vial. The morphs differed significantly in the calyx cross-section area of primary polyps. Despite being considered a single species according to skeletal based taxonomy, the significant ecological and molecular differences between pink and orange C. gracilis specimens suggest that they may belong to separate species.     

Induction of settlement and metamorphosis in the sand dollarEchinarachnius parma: Evidence for an adult-associated factor

Larvae of the northern sand dollarEchinarachnius parma (Lamarck), reared from adults collected from Eagle Head, Nova Scotia, Canada, in 1988 and 1989, metamorphose in significantly greater numbers on sand conditioned by adults than on non-conditioned sand. The metamorphic factor has a molecular weight < 1000 and is destroyed by heating. Larvae are capable of sensing this cue in the water column under static conditions. Substrata of varying particle size and surface texture can be conditioned by adults to induce metamorphosis. Substrata conditioned in the dark, and conditioned sand treated with antibiotics also induce metamorphosis suggesting that the factor is not produced by adult-associated bacteria or microflora. In nature, this adult-associated factor may direct settlement of larvae to established sand dollar beds resulting in the aggregated distribution of this species.     

Food limitation stimulates metamorphosis of competent larvae and alters postmetamorphic growth rate in the marine prosobranch gastropodCrepidula fornicata

The effects of food limitation on growth rates and survival of marine invertebrate larvae have been studied for many years. Far less is known about how food limitation during the larval stage influences length of larval life or postmetamorphic performance. This paper documents the effects of food limitation during larval development (1) on how long the larvae ofCrepidula fornicata (L.) can delay metamorphosis in the laboratory after they have become competent to metamorphose and (2) on postmetamorphic growth rate. To assess the magnitude of nutritional stress imposed by different food concentrations, we measured growth rates (as changes in shell length and ash-free dry weight) for larvae reared in either 0.45-m filtered seawater or at phytoplankton concentrations (Isoehrysis galbana, clone T-ISO) of 1 × l0³, 1 × 10⁴, or 1.8 × 10⁵ cells ml^–1. Larvae increased both shell length and biomass at 1 × 10⁴ cells ml^–1, although significantly more slowly than at the highest food concentration. Larvae did not significantly increase (p > 0.10) mean shell length in filtered seawater or at a phytoplankton concentration of only 1 × 10³ cells ml^–1, and in fact lost weight under these conditions. To assess the influence of food limitation on the ability of competent individuals to postpone metamorphosis, larvae were first reared to metamorphic competence on a high food concentration ofI. galbana (1.8 × 10⁵ cells ml^–1). When at least 80% of subsampled larvae were competent to metamorphose, as assessed by the numbers of indlviduals metamorphosing in response to elevated K⁺ concentration in seawater, remaining larvae were transferred either to 0.45-m filtered seawater or to suspensions of reduced phytoplankton concentration (1 × 10³, 1 × 10⁴, or 5 × 10⁴ cells ml^–1), or were maintained at 1.8 × 10⁵ cells ml^–1. All larvae were monitored daily for metamorphosis. Individuals that metamorphosed in each food treatment were transferred to high ration conditions (1.8 × 10⁵ tells ml^–1) for four additional days to monitor postmetamorphic growth. Competent larvae responded to all food-limiting conditions by metamorphosing precociously, typically 1 wk or more before larvae metamorphosed when maintained at the highest food ration. Surprisingly, juveniles reared at full ration grew more slowly if they had spent 2 or 3 d under food-limiting conditions as competent larvae. The data show that a rapid decline in phytoplankton concentration during the larval development ofC. fornicata stimulates metamorphosis, foreshortening the larval dispersal period, and may also reduce the ability of postmetamorphic individuals to grow rapidly even when food concentrations increase.     

The marine bacterium Alteromonas espejiana induces metamorphosis of the hydroid Hydractinia echinata

The marine hydroid Hydractinia echinata develops into a primary polyp from a planula larva stage. The planula does not undergo metamorphosis in sterile filtered seawater. Metamorphosis is induced by certain bacteria occurring, as a rule, on the shells of molluscs inhabited by hermit crabs of the genus Eupagurus. Bacteria were isolated from shells occupied by H. echinata, and bacterial clones were selected which had a strong potency for inducing metamorphosis in planula larvae. One such clone was further subcloned for strong metamorphosis-inducing potency and finally investigated for inductive characteristics and for identification purposes. The bacterium is a motile, aerogen, gram-negative rod with a polar flagellum. It was identified on the basis of several physiological characteristics as a strain of the genus Alteromonas espejiana. The ability to induce metamorphosis might not be restricted to A. espejiana. The inhibitor of protein kinase C, sphingosine, inhibited metamorphosis induced by A. espejiana. The metamorphosis-inducing principle is likely to be a lipid, since upon lipid extraction and separation of different lipid classes by solid phase extraction on silica-aminopropyl columns a metamorphosis-inducing fraction was obtained.     

Marginal tentacles of the corallimorpharian Rhodactis rhodostoma. 2. Induced development and long-term effects on coral competitors

Polyps of the corallimorpharian Rhodactis rhodostoma (Ehrenberg, 1934) form aggregations that monopolise patches of space on the shallow reef flats of some Red Sea coral reefs. Some of these polyps bear specialised bulbous marginal tentacles (BMTs) where they contact cnidarian competitors. BMTs differ from the normally filiform marginal tentacles (FMTs) of R. rhodostoma, and appear to develop from them. However, their morphogenesis and long-term impacts on spatial competition with reef corals are unknown. We experimentally induced contacts between R. rhodostoma polyps and colonies of the branching stony coral Acropora eurystoma on a shallow coral reef at Eilat, northern Red Sea. During the first 24 d of contact, the A. eurystoma colonies extruded mesenterial filaments that damaged the tissues of the corallimorpharian polyps. After 18 d,>90% of R. rhodostoma individuals had developed BMTs, which resulted in a reversal in the direction of competitive damage. During the subsequent 1.5 years of observation, the corallimorpharians maintained well-developed BMTs, unilaterally damaged the tissues of A. eurystoma, and in some cases moved onto the stony coral skeletons and partially overgrew them. BMTs developed from FMTs in a series of four distinct stages, accompanied by significant changes in their morphology, cnidom, and density of nematocysts. Isolated control polyps did not develop BMTs or show any signs of damage. In contrast, corallimorpharian polyps transplanted into contact with colonies of the massive stony coral Platygyra daedalea began to develop sporadic BMTs, but were unilaterally and severely damaged by the corals, and started to disappear within 21 d, after the corals developed sweeper tentacles. We conclude that long-term outcomes of competition between R. rhodostoma and reef-building corals depend largely on the relative aggressive reach of the competitive mechanisms developed by each species. As a consequence, this corallimorpharian is an intermediate competitor in the aggressive hierarchy among Indo-Pacific reef corals. This study confirms that R. rhodostoma polyps may actively damage and overgrow some stony corals, leading to the formation of an almost continuous blanket of polyps in large patches of some shallow reef flats. Received: 15 July 1998 / Accepted: 24 March 1999