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.     

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.     

Bioluminescence of deep-sea coronate medusae (Cnidaria: Scyphozoa)

Bioluminescence is the production of visible light by a living organism. The light commonly appears as flashes from point sources (involving one or more cells, usually described as photocytes) or as a glandular secretion. A visible flash usually involves synchronous light emission from a group of cells or, if from a single-celled organism such as a dinoflagellate, from a group of organelles. The number of cells (or organelles) responding synchronously is the main determinant of the flash intensity. Bioluminescence is a common phenomenon in many deep-sea animals and is widespread among the Cnidaria. In this paper, we compare and contrast in situ and laboratory recordings of the bioluminescent responses of specimens of the deep-sea scyphozoans Atolla wyvillei, Atolla vanhoffeni, Atolla parva, Nausithoe rubra, Paraphyllina intermedia, Periphyllopsis braueri and Periphylla periphylla. Displays in all seven species consist of localised flashes and propagated waves of light in the surface epithelium. The first few single waves propagate at rates of up to 60 cm s^-1 but subsequent ones in any sequence of stimuli gradually decrease in speed. After several single wave responses, a subsequent stimulus may elicit multiple waves that persist for several seconds. Following such a frenzy, the specimen becomes temporarily refractory to further stimuli, but if rested will recover its normal responses and may produce further frenzies. The dome area, situated above the coronal groove, of the genera Paraphyllina, Periphylla, and Nausithoe is covered with luminescent point sources. Such point sources are generally absent from the dome of species of Atolla. Captured specimens of A. parva also produce secretory bioluminescence, corroborating prior in situ observations of this ability. Secretory bioluminescence in P. periphylla takes the form of scintillating particles released from the lappet margins. We did not observe secretory displays in specimens of any other species in the laboratory, but one instance of apparent secretory luminescence was recorded in situ in a specimen of A. wyvillei.Communicated by J. P. Thorpe, Port Erin     

The morphogenesis of ephyra in Coronatae (Cnidaria,Scyphozoa)

The morphogenesis of ephyrae of Atorella vanhoeffeni Bigelow, 1909 (Werner, 1967) and of Nausithoe maculata Jarms, 1990 during strobilation is described. We found differences in the developmental pattern of marginal structures and structural changes of longitudinal muscle tubes in particular. During strobilation the polyp’s tetraradiate symmetry is passed to the ephyra of both taxa as a tetraradiate central symmetry that we consider a major plesiomorphic character. The present results also indicate divergent patterns of ephyra development during strobilation that lead to variable marginal symmetries of ephyrae and thus of medusae. Therefore, the marginal symmetry of medusae of N. maculata is octoradiate and of A. vanhoeffeni is hexaradiate. We conclude the latter is stated as derived pattern. These results lead us to maintain both families Nausithoidae and Atorellidae.     

Carbon metabolism and strobilation in Cassiopea andromedea (Cnidaria: Scyphozoa): Significance of endosymbiotic dinoflagellates

Scyphopolyps and scyphomedusae of Cassiopea andromeda Forskål (Cnidaria, Scyphozoa) containing dinoflagellate endosymbionts (zooxanthellae) were investigated for rates and pathways of carbon fixation. Photosynthesis by the algae, accounting for 80 and 15 mol C h^-1 on a dry weight basis in medusae and polyps, respectively, by far exceeds dark incorporation of inorganic carbon by the intact association. Photosynthetic carbon fixation is operated via C₃ pathway of carbon reduction. DCMU-treatment (1×10^-6 M and 1×10^-5 M) completely inhibits light-dependent carbon assimilation. Major photosynthates presumably involved in a metabolite flow from algal symbionts to animal tissue are glycerol and glucose. A total of 5–10% net algal photosynthate appears to be seleased in vivo to the host. This is probably less than the energy supply ultimately required for the nutrition of the polyps and medusae. The presence of zooxanthellae proved to be indispensable for strobilation in the scyphopolyps. However, photosynthesis by algal symbionts as well as photosynthate release is obviously not essential for the initiation of ephyrae as is shown by DCMU-treatment, culture in continous darkness, and aposymbiotic controls. It is therefore concluded that strobilation is supported, but not triggered by algal photosynthetic activity. The induction of strobilation thus seems to depend on a more complex system of regulation.     

Organ-like gonads, complex oocyte formation, and long-term spawning in Periphylla periphylla (Cnidaria, Scyphozoa, Coronatae)

An account is given about the development of the gametes of the holopelagic coronate scyphomedusa Periphylla periphylla (Péron and Lesueur 1809). The gonads of the species are complex and differ from those thus far described in Scyphozoa in having this characteristic composition of trophocytes, follicle cells, gamete-releasing pores, mucus cells, and resorption cells. Our results differ from those of previous coronate studies with respect to the contact of the oocytes with the gonad tissue throughout the duration of development. Among the Medusozoa, follicle cells have thus far been considered as an apomorphy for the Staurozoa, but their presence in the Scyphozoa casts some doubts on this assumption. From morphological structure and examination of the gonads and gametes, it can be deduced that P. periphylla has true organs and that gamete release is continuous. These results supplement our knowledge of the reproductive biology of this mesopelagic species.     

Ovarian morphology and oogenesis in Aurelia aurita (Scyphozoa: Semaeostomae): ultrastructural evidence of heterosynthetic yolk formation in a primitive metazoan

In Aurelia aurita, the ovaries arise as horseshoe-shaped evaginations of the gastrodermis in the floor of four interradial gastric pouches. Germ-cell islands arise within endodermally-derived gastrodermal cells. Oocytes grow and gradually bulge into the mesoglea while maintaining physical contact throughout vitellogenesis with specialized cells called trophocytes. Ultrastructural changes suggest that these cells transport yolk precursors from the coelenteron to the oocytes in a manner similar to that reported for the trophonema cells of anthozoan ovaries. Vitellogenesis involves both the autosynthetic activity of the oocyte organelles (Golgi complex and rough endoplasmic reticulum) and the heterosynthetic incorporation of precursors through endocytotic processes involving both coated pits and vesicles and smooth-surfaced tubules. Ultrastructural data suggest that different types or classes of yolk precursors enter the oocyte through the trophocytes and via the surrounding mesoglea. To our knowledge, this is the most primitive animal in which this type of yolk synthesis has been described. The trophocyte-oocyte relationship in oocytes of A. aurita is reminiscent of the trophonema-oocyte relationship in anthozoans and supports the belief that the Anthozoa and Scyphozoa share a close phylogenetic relationship.     

Predatory behavior ofPhacellophora camtschatica and size-selective predation uponAurelia aurita (Scyphozoa: Cnidaria) in Saanich Inlet,British Columbia

Predation uponAurelia aurita byPhacellophora camtschatica was studied by SCUBA divers in a fjord in British Columbia between July and September 1986. The behavior and size ofP. camtschatica affected their foraging success. Larger predators captured more and larger prey. The size and behavior of the prey also affected the probability of capture. Predators were found at densities which can affect both the size composition and the overall numbers of the prey population.     

Substrate choice and settlement preferences of planula larvae of five Scyphozoa (Cnidaria) from German Bight,North Sea

The settlement behaviour of planula larvae and their development to young polyps was investigated in laboratory experiments in five scyphozoan species [Aurelia aurita (L.), Cyanea capillata (L.), Cyanea lamarckii Péron and Leseur, Chrysaora hysoscella (L.), and Rhizostoma octopus (L.)]. The undersides of settling plates were strongly preferred for settlement. Shells, the only natural substrate type offered, were less attractive than artificial substrates (concrete, machined wood, polyethylene, and glass). The advantages of colonization of substrate undersides for survival and reproduction of polyps are discussed. It is supposed that the increase of artificial substrates in our seas, due to marine litter pollution and submarine building activities, enlarge the areas of distribution of scyphozoan polyps, in coastal as well as in off-shore regions. Subsequent increases in ephyra production by polyps are probably one reason for the increase in mass occurrences of jellyfish recognized worldwide during the last few decades. It is suggested that the early developmental stages in the cnidarian life cycle, the planula larvae, and the polyps, play the key role in the development of jellyfish outbursts.     

Recent strandings of the giant jellyfish Rhizostoma luteum Quoy and Gaimard, 1827 (Cnidaria: Scyphozoa: Rhizostomeae) on the Atlantic and Mediterranean coasts

We present reports of sightings of living and stranded specimens of Rhizostoma luteum on the Atlantic coast of Morocco and along the south shore of the Iberian Peninsula in June–July 2012 and in January–February 2013. During summer 2012 and following the dominant currents, the jellyfish first appeared in the Gulf of Cadiz west of the Strait of Gibraltar. Subsequently, seven additional sightings were reported east of the Strait, in the Alboran Sea. In winter 2013, another event of stranded individuals of this species occurred in the Gulf of Cadiz. A phylogenetic analysis performed on the mitochondrial cytochrome c oxidase I (COI) gene sequence in specimens from both stranding events confirmed the morphological classification, ratifying that R. luteum differs from Rhizostoma octopus and Rhizostoma pulmo. This study records the presence of this species for the first time in 60 years.     

Comparison of the statolith structures of <Emphasis Type=Italic>Chironex fleckeri</Emphasis> (Cnidaria,Cubozoa) and <Emphasis Type=Italic>Periphylla periphylla</Emphasis> (Cnidaria,Scyphozoa): a phylogenetic approach

The rhopalia and statocysts of Periphylla periphylla (Péron and Lesueur in Ann Mus Hist Nat Marseille 14:316–366,1809) and Chironex fleckeri Southcott (Aust J Mar Freshw Res 7(2):254–280 1956) were examined histologically and showed several homologous characteristics. Differences in sensory area distribution could be connected to a slightly different functionality of equilibrium sensing. In P. periphylla, the statoliths (crystals) grow independently of each other; whereas in C. fleckeri, one large crystal covers the smaller ones. The structures of both statoliths were examined in detail with single-crystal diffraction, microtomography and diffraction contrast tomography. The single compact statolith of C. fleckeri consisted of bassanite as was previously known only for other rhopaliophoran medusae. An origin area with several small oligocrystals was located in the centre of the cubozoan statolith. The origin areas and the accretion of statoliths are similar in both species. Our results lead to the assumption that the single bassanite statolith of C. fleckeri (Cnidaria, Cubozoa) is a progression of the scyphozoan multiplex statolith. It is therefore suggested that the Cubozoa are derived from a scyphozoan ancestor and are a highly developed taxa within the Rhopaliophora.     

Morphology and development of benthic and pelagic life stages of North Sea jellyfish (Scyphozoa, Cnidaria) with special emphasis on the identification of ephyra stages

Jellyfish blooms or invasions could be detected in an early phase of development if the youngest medusa stages (ephyrae) and their early growth stages (post-ephyrae) were identifiable in plankton samples but a useful identification key for ephyrae in early growth stages is lacking for most species. In the present study, the identification characteristics of adult North Sea scyphomedusae (Aurelia aurita, Cyanea capillata, Cyanea lamarckii, Chrysaora hysoscella, Rhizostoma octopus) collected around the island of Helgoland (German Bight) in July?CAugust 2003 and 2004 are described. Planula larvae were measured and reared to polyps in the laboratory. The process of ephyrae development asexually produced by the polyps (strobilation) was photo-documented. Photographs of the ephyrae growth stages were combined with drawings of features useful for the species identification. The provided identification key allows discrimination among post-ephyrae from plankton samples, probably leading to conclusions on the development of jellyfish blooms and their causes.     

Some carotenoids in the jelly-fish Aurelia aurita (Scyphozoa: Discomedusae)

The author investigated the carotenoids in the jelly-fish Aurelia aurita (L.), from the Baltic Sea. By means of columnar and thin-layer chromatography, the following carotenoids were found to be present in that species: -carotene, echinenone isocryptoxanthin, canthaxanthin, lulein, zeaxanthin, astaxanthin and astacene.     

Hebella parasitica (Cnidaria,Hydroida): A thecate polyp producing an anthomedusa

The thecate hydroid Hebella parasitica (Ciamician), reared under controlled conditions, produced an ephemerous medusa with gonads on the manubrium. This feature does not agree with the current classification of hydroids, according to which a thecate polyp is expected to produce a medusa with gonads on its radial canals. As no data on the reproduction of other species of Hebella are available, the systematic position of H. parasitica should be considered uncertain.Work done within the Finalized Project Oceanografia e i fondi marini, sub-project Risorse biologiche of the C.N.R.     

Swimming and feeding in Periphylla periphylla (Scyphozoa, Coronatae)

Some western Norwegian fjords host extraordinarily abundant and persistent populations of the mesopelagic, coronate scyphomedusa, Periphylla periphylla. In these environments, from late autumn to spring, the medusae undertake regular diel vertical migrations into surface waters. From unique observations obtained with a remotely operated vehicle (ROV), including observations made without artificial light, we observed that 90% of the medusae swam with their tentacles in aboral position. Stomach content analyses of surface-collected specimens revealed that the medusae ate mainly calanoid copepods, but ostracods and large euphausiids were also prominent components of their diets. The clearance rate potential of P. periphylla, assessed from in situ observations and stomach contents, was comparable to that of similar-sized, epipelagic gelatinous species. Our findings suggest that P. periphylla behave as active predators in surface waters.     

Laboratory observations on the life history of Rhopilema verrilli (Scyphozoa: Rhizostomeae)

The life history of the scyphozoan Rhopilema verrilli is described from the planula to the young medusa stages. Planulae are retained within the gonadal tissue of the medusa until fully developed. On liberation, most planulae set and developed into small scyphistomae within 7 to 10 days. The scyphistoma differs from those of other described species in having an unusually large, clavate manubrium. The only means of asexual reproduction observed in the scyphistoma cultures involved the formation of podocysts. Strobilation was usually of the monodisc variety, although polydics strobilation was not infrequent. The process of strobilation was completed within 7 days at 20°C. Newly liberated ephyrae typically had 8 pairs of lappets, and 8 rhopalia. Ephyral development resembled that of the closely related rhizostome Rhizostoma pulmo. The cnidome of the planula and scyphistoma consisted of atrichous isorhizas (a atrichs) and microbasic heterotrichous euryteles, while that of the strobila and ephyra consisted of a atrichs, euryteles, and holotrichous haplonemesContribution No. 546 from the Virginia Institute of Marine Science, Gloucester Point, Virginia 23062, USA.     

Life history and settlement preferences of the edible jellyfish Catostylus mosaicus (Scyphozoa: Rhizostomeae)

 The life history and settlement preferences of larvae of Catostylus mosaicus (Scyphozoa: Rhizostomeae) (Quoy and Gaimard, 1824) were investigated in New South Wales, Australia, over a 2 mo period beginning in November 1998. The life history consisted of an alternation between a sexual, medusoid stage and an asexual, polypoid stage, and was similar to that described for other rhizostomes. Planula larvae were brooded by the adults. Approximately 4 d after collection, larvae settled on a variety of substrata including wood, sandstone, shell, seagrass and glass, and metamorphosed into four-tentacled polyps. The number of tentacles increased and polyps strobilated when they had between 12 and 20 tentacles. Strobilation occurred within 15 d of settlement, but only polyps that settled on the concave surfaces of the shells strobilated. Both monodisk and polydisk strobilation was observed. Ephyrae were raised for one month and were observed developing oral arms. Polyps reproduced asexually via the formation of podocysts, by production of buds, and by partial fission. Received: 30 April 1999 / Accepted: 27 August 1999     

Derivation of the reduced life cycle of <Emphasis Type="Italic">Thecoscyphus zibrowii</Emphasis> Werner, 1984 (Cnidaria,Scyphozoa)

The species Thecoscyphus zibrowii Werner, 1984 has an exceptional life cycle, which lacks a medusa stage but develops an extraordinary structure (egg sac) for reproduction. Investigation of the life cycle, as well as anatomical and histological studies of the different developmental stages of T. zibrowii were performed to provide evidence for a possible homology of the egg sac with the medusa stage and to determine whether the reduced metagenesis of T. zibrowii is derived from strobilation. The egg sac showed several characteristics, which were compared to those of coronate medusae. The ectodermis of the egg sac had a plate-like appearance and was completely ciliated as is typical for coronate medusae. The number and the location of the gonads were similar to those of coronate medusae. The cnidocysts were significantly larger in the egg sac than in the polyp. A size difference of cnidocysts in the medusa and the polyp stage is known for several Coronatae. Characteristics of egg sac formation were compared to characteristics of strobilation. The formation of the early operculum was similar in T. zibrowii and N. eumedusoides. The constriction of egg sac and strobila occurred in the same mode and the gastric cavities of two egg sacs stayed in contact in a similar fashion to the gastric cavities of the strobila discs. The developmental zones of cnidoblasts of the egg sac and polyp were separated during the formation of the egg sac which showed a similar developmental gradient to a strobila. The existence of all of these consistent characteristics makes it very likely that the egg sac structure was homologous to a medusa. The species T. zibrowii would therefore be derived from a metagenetic ancestor. This species has reduced the medusa generation to the greatest extent within the Nausithoidae and has demonstrated thus far the endpoint of a regressive evolution of the medusa generation.