Early Life History of the ‘Irukandji’ Jellyfish Carukia barnesi

Adult medusae of Carukia barnesi were collected near Double Island, North Queensland Australia. From 73 specimens, 8 males and 15 females spawned under laboratory conditions. These gametes were artificially mixed which resulted in fertilized eggs. Post fertilization, most eggs developed to an encapsulated planula stage and then paused for between six days and six months prior to hatching as ciliated planulae. The paused stage planulae were negatively buoyant and adhered to substrate. The first planula was produced six days post fertilization, lacked larval ocelli, remained stationary, or moved very slowly for two days prior to metamorphosis into primary polyps. Mature polyps reproduced through asexual reproduction via lateral budding producing ciliated swimming polyps, which in turn settled and developed into secondary polyps. Medusae production for this species was in the form of monodisc strobilation, which left behind polyps able to continue asexual reproduction.     

Pre-exposure to simultaneous,but not individual,climate change stressors limits acclimation capacity of Irukandji jellyfish polyps to predicted climate scenarios

Researchers have investigated the immediate effects of end-of-century climate change scenarios on many marine species, yet it remains unclear whether we can reliably predict how marine species may respond to future conditions because biota may become either more or less resistant over time. Here, we examined the role of pre-exposure to elevated temperature and reduced pH in mitigating the potential negative effects of future ocean conditions on polyps of a dangerous Irukandji jellyfish Alatina alata. We pre-exposed polyps to elevated temperature (28 °C) and reduced pH (7.6), in a full factorial experiment that ran for 14 d. We secondarily exposed original polyps and their daughter polyps to either current (pH 8.0, 25 °C) or future conditions (pH 7.6, 28 °C) for a further 34 d to assess potential phenotypic plastic responses and whether asexual offspring could benefit from parental pre-exposure. Polyp fitness was characterised as asexual reproduction, respiration, feeding, and protein concentrations. Pre-exposure to elevated temperature alone partially mitigated the negative effects of future conditions on polyp fitness, while pre-exposure to reduced pH in isolation completely mitigated the negative effects of future conditions on polyp fitness. Pre-exposure to the dual stressors, however, reduced fitness under future conditions relative to those in the control treatment. Under future conditions, polyps had higher respiration rates regardless of the conditions they were pre-exposed to, suggesting that metabolic rates will be higher under future conditions. Parent and daughter polyps responded similarly to the various treatments tested, demonstrating that parental pre-exposure did not confer any benefit to asexual offspring under future conditions. Importantly, we demonstrate that while pre-exposure to the stressors individually may allow Irukandji polyps to acclimate over short timescales, the stressors are unlikely to occur in isolation in the long term, and thus, warming and acidification in parallel may prevent polyp populations from acclimating to future ocean conditions.

     

Telomerase activity is not related to life history stage in the jellyfish Cassiopea sp.

The polyp (scyphistoma) of the jellyfish Cassiopea sp. can be maintained in culture for a long time, as polyps repeatedly reproduce asexually via formation of vegetative buds or propagules. The medusa, which is the sexually reproducing stage, typically has a relatively short life span. As a first step to understand the difference in life spans of the polyp and medusa stages of Cassiopea sp., we measured telomerase activity in different life cycle stages. We found telomerase activity in tissues of aposymbiotic polyps and propagules and symbiotic ephyrae (newly budded medusae) and adult medusae. No significant difference in telomerase activity was found between polyps and the bell region of the medusae. The cloned elongation products of the stretch PCR contained the TTAGGG repeats suggesting that the jellyfish has the ‘vertebrate’ telomere motif (TTAGGG)_n. This is the first study to show that somatic tissues of both polyp and medusa stages of a cnidarian had telomerase activity. Telomerase activity in somatic tissues may be related to the presence of multipotent interstitial cells and high regenerative capacity of cnidarians.     

Is the remodeling of the polyp prepattern in a hydrozoan planula a function of larval age or size and is it of “adaptive” significance?

Eggs of medusae develop into lecithotrophic planulae that undergo metamorphosis at different ages to form polyps. As planulae age they decrease in size as their yolk stores are utilized. The planulae of most Phialidium medusae develop into polyps where there is a decrease in the size of the holdfast region and a relative increase in the size of the hydranth region as they age. These changes occur independently of the decrease in planula size. In planulae with a decrease in the size of the holdfast region and an increase in the size of the hydranth-forming region there was a 50% decline in polyps that successfully stayed attached to the substrate after metamorphosis. These aged planulae produced an initial hydranth with the same number of tentacles as polyps from full-sized young planulae while young half-sized planulae produced hydranths where the tentacle number was smaller. The first phase of polyp colony growth with a small initial hydranth was slower than growth of a colony with a larger initial hydranth. Predation during this period led to more death in colonies with a small initial hydranth. The decline in successful attachment in aged planulae was not offset by the higher rate of growth and a smaller window of time where predation leads to death, suggesting that this age-related developmental change in planulae was not adaptive.     

Fine structure, histochemistry, and morphogenesis during excystment of the podocysts of the giant jellyfish Nemopilema nomurai (Scyphozoa, Rhizostomeae)

Production of podocysts is the exclusive form of asexual reproduction by polyps of the giant jellyfish Nemopilema nomurai, which has been recurrently blooming in the East Asian seas in the last decade. Podocycts consist of a dome-shaped chitinous capsule with laminated structure that encapsulates a mass of cyst cells filled with granules containing nutrient reserves such as proteins, carbohydrates, and lipids. Mitochondria, rough endoplasmic reticulum, and Golgi complexes are scarce in the cytoplasm of these cells, and the staining reaction for RNA is weak, indicating very low metabolic activity. Podocysts are capable of dormancy for at least 5 years without significant change of internal structure or nutrient reserves. Integrated information about spontaneous and artificially induced metamorphosis suggests that the following processes occur during excystment: (1) nematocyst formation in the internal cell mass, (2) stratification of the cell mass into endoderm and ectoderm, (3) extrusion of the cell mass through a gradual opening of the capsule, (4) formation of primordial polyp mouth and tentacles, and (5) metamorphosis to a polyp. We morphologically confirmed that N. nomurai podocysts have the capacity for long-term dormancy, an ability that should contribute to the periodic nature of the massive blooms of medusae of this species.     

Life Cycle Reversal in Aurelia sp.1 (Cnidaria,Scyphozoa)

The genus Aurelia is one of the major contributors to jellyfish blooms in coastal waters, possibly due in part to hydroclimatic and anthropogenic causes, as well as their highly adaptive reproductive traits. Despite the wide plasticity of cnidarian life cycles, especially those recognized in certain Hydroza species, the known modifications of Aurelia life history were mostly restricted to its polyp stage. In this study, we document the formation of polyps directly from the ectoderm of degenerating juvenile medusae, cell masses from medusa tissue fragments, and subumbrella of living medusae. This is the first evidence for back-transformation of sexually mature medusae into polyps in Aurelia sp.1. The resulting reconstruction of the schematic life cycle of Aurelia reveals the underestimated potential of life cycle reversal in scyphozoan medusae, with possible implications for biological and ecological studies.     

Polypengeneration und Entwicklungsgeschichte vonEucheilota maculata (Thecata-Leptomedusae)

Polyps and medusae differ in regard to habitats, evolution, and morphological structures. In order to replace the former taxonomic systems which deal with polyp and medusa generations separately, by a single valid classification including both generations, knowledge of all essential life history phases is necessary. Modern methods of culturing marine hydroids are outlined briefly. Successful culturing provides the means to link formerly unidentified polyps or medusae with one another. The present paper is concerned with the hydroidEucheilota maculata Hartlaub, the medusa of which is common in the southern North Sea. The polyps formerly unknown have been reared from fertilized eggs of the medusae. They were raised to full size, formed colonies, and produced gonangia and medusae. Thus the morphology of the single polyp, the polyp colony, and of the young medusa could be investigated in detail. The nematocyst equipment of the two generations and of all developmental stages is described as well as the number of chromosomes. The systematic position of the genusEucheilota is discussed and the diagnosis of the speciesE. maculata, including the two generations, given.     

Effects of pH on asexual reproduction and statolith formation of the scyphozoan, <Emphasis Type="Italic">Aurelia labiata</Emphasis>

Although anthropogenic influences such as global warming, overfishing, and eutrophication may contribute to jellyfish blooms, little is known about the effects of ocean acidification on jellyfish. Most medusae form statoliths of calcium sulfate hemihydrate that are components of their balance organs (statocysts). This study was designed to test the effects of pH (7.9, within the average current range, 7.5, expected by 2100, and 7.2, expected by 2300) combined with two temperatures (9 and 15°C) on asexual reproduction and statolith formation of the moon jellyfish, Aurelia labiata. Polyp survival was 100% after 122 d in seawater in all six temperature and pH combinations. Because few polyps at 9°C strobilated, and temperature effects on budding were consistent with published results, we did not analyze data from those three treatments further. At 15°C, there were no significant effects of pH on the numbers of ephyrae or buds produced per polyp or on the numbers of statoliths per statocyst; however, statolith size was significantly smaller in ephyrae released from polyps reared at low pH. Our results indicate that A. labiata polyps are quite tolerant of low pH, surviving and reproducing asexually even at the lowest tested pH; however, the effects of small statoliths on ephyra fitness are unknown. Future research on the behavior of ephyrae with small statoliths would further our understanding of how ocean acidification may affect jellyfish survival in nature.     

Irukandji jellyfish polyps exhibit tolerance to interacting climate change stressors

Increasing ocean temperatures and strengthening boundary currents have caused the poleward migration of many marine species. Cubozoan jellyfish known to cause Irukandji syndrome have historically been confined to tropical waters but may be expanding into subtropical regions. Here, we examine the interactive effects of warming and acidification on the population dynamics of polyps of an Irukandji jellyfish, Alatina nr mordens, and the formation of statoliths in newly metamorphosed medusae, to determine if this jellyfish could tolerate future conditions predicted for southeast Queensland (SEQ), Australia. Two experiments, examining the orthogonal factors of temperature and pH, were undertaken. Experiment 1 mimicked the current, ca. 2050 and ca. 2100 summer temperature and pH conditions predicted for SEQ using A1F1 scenarios (temperature: 25, 27, 29 °C; pH: 7.9, 7.8, 7.6) and Experiment 2 mimicked current and future winter conditions (18 and 22 °C, pH 7.9, 7.8, 7.6). All polyps in Experiment 1 survived and budded. Fewer polyps budded in the lower pH treatments; however, patterns varied slightly among temperature treatments. Statoliths at pH 7.6 were 24% narrower than those at pH 7.8 and 7.9. Most polyps survived the winter conditions mimicked by Experiment 2 but only polyps in the 22 °C, pH 7.9 treatment increased significantly. The current absence of A. nr mordens medusae in SEQ, despite the polyps' ability to tolerate the current temperature and pH conditions, suggests that ecological, rather than abiotic factors currently limit their distribution. Observations that budding was lower under low pH treatments suggest that rates of asexual reproduction will likely be much slower in the future. We consider that A. nr mordens polyps are likely to tolerate future conditions but are unlikely to thrive in the long term. However, if polyps can overcome potential ecological boundaries and acidification proceeds slowly A. nr mordens could expand polewards in the short term.     

Cell Proliferation in Cubozoan Jellyfish Tripedalia cystophora and Alatina moseri

Cubozoans (box jellyfish) undergo remarkable body reorganization throughout their life cycle when, first, they metamorphose from swimming larvae to sessile polyps, and second, through the metamorphosis from sessile polyps to free swimming medusae. In the latter they develop complex structures like the central nervous system (CNS) and visual organs. In the present study several aspects of cell proliferation at different stages of the life cycle of the box jellyfish Tripedalia cystophora and Alatina moseri have been examined through in vivo labeling of cells in the synthetic phase (S phase) of the cell cycle. Proliferation zones were found in metamorphosing polyps, as well as in juvenile medusae, where both the rhopalia and pedalia have enhanced rates of proliferation. The results also indicate a rather fast cell turnover in the rhopalia including the rhopalial nervous system (RNS). Moreover, T. cystophora showed diurnal pattern of cell proliferation in certain body parts of the medusa, with higher proliferation rates at nighttime. This is true for two areas in close connection with the CNS: the stalk base and the rhopalia.     

Sexual Reproduction and Seasonality of the Alaskan Red Tree Coral,Primnoa pacifica

The red tree coral Primnoa pacifica is an important habitat forming octocoral in North Pacific waters. Given the prominence of this species in shelf and upper slope areas of the Gulf of Alaska where fishing disturbance can be high, it may be able to sustain healthy populations through adaptive reproductive processes. This study was designed to test this hypothesis, examining reproductive mode, seasonality and fecundity in both undamaged and simulated damaged colonies over the course of 16 months using a deepwater-emerged population in Tracy Arm Fjord. Females within the population developed asynchronously, though males showed trends of synchronicity, with production of immature spermatocysts heightened in December/January and maturation of gametes in the fall months. Periodicity of individuals varied from a single year reproductive event to some individuals taking more than the 16 months sampled to produce viable gametes. Multiple stages of gametes occurred in polyps of the same colony during most sampling periods. Mean oocyte size ranged from 50 to 200 µm in any season, and maximum oocyte size (802 µm) suggests a lecithotrophic larva. No brooding larvae were found during this study, though unfertilized oocytes were found adhered to the outside of polyps, where they are presumably fertilized. This species demonstrated size-dependent reproduction, with gametes first forming in colonies over 42-cm length, and steady oocyte sizes being achieved after reaching 80-cm in length. The average fecundity was 86 (±12) total oocytes per polyp, and 17 (±12) potential per polyp fecundity. Sub-lethal injury by removing 21–40% of colony tissue had no significant reproductive response in males or females over the course of this study, except for a corresponding loss in overall colony fecundity. The reproductive patterns and long gamete generation times observed in this study indicate that recruitment events are likely to be highly sporadic in this species increasing its vulnerability to anthropogenic disturbances.     

Phenotypic plasticity in hydrozoans: morph reversibility.

The life cycle of Hydrozoans typically comprises two phases: the polyp, either solitary or colonial, with generally a benthic habitat, and the medusa which lives in the plankton. In its typical metagenetic cycle, the medusa is budded from the polyp, which is the product of sexual reproduction of medusae. However, several alternative reproduction patterns have also been described. In particular some species are able to perform a regressive transformation of the medusae that transform themselves into polyps bypassing sexual reproduction. In a species with alternative morphs switched by the environment, the more labile is the correlation between environmental factors acting on the genetic switch and the factors to which the resulting form is adapted, the more hazardous will be the development of either body form. However, we can explain the evolutionary advantage offered by reversion between morphs of these plastic species living in shallow water unpredictable environments: should produced medusae be released in the "wrong" environment, they would still have a chance of survival under another form.     

Effects of low dissolved oxygen on survival and asexual reproduction of scyphozoan polyps (Chrysaora quinquecirrha)

Hypoxic conditions are common in many coastal environments such as Chesapeake Bay. While medusae appear to be quite tolerant of low dissolved oxygen (DO) concentrations, the effects of hypoxia on the benthic polyp stages are unknown. Chrysaora quinquecirrha (DeSor) polyps, and were subjected to 5 DO treatments (air-saturated [control], 3.5, 2.5, 1.5 and 0.5 mg l^–1) in the laboratory. Polyp survival and development were documented over 24 d. Virtually no mortality occurred in any treatment during the first 5 d. Total polyp mortality after 24 d was 59.3% at the lowest DO concentration, whereas <3% mortality was observed in the air-saturated treatment. Formation of stolons and strobilae occurred in all treatments, however, the proportions of polyps undergoing stolonation and strobilation were significantly greater in all DO concentrations above 0.5 mg l^–1. Polyp encystment was not observed in any treatment over the course of the 24 d experiment. These results indicate that polyps can survive and asexually propagate even during prolonged exposure to hypoxic conditions.     

Effects of low salinity on settlement and strobilation of scyphozoa (Cnidaria): Is the lion’s mane <Emphasis Type="Italic">Cyanea capillata</Emphasis> (L.) able to reproduce in the brackish Baltic Sea?

Several species of scyphozoan medusae occur in river estuaries and other brackish waters but it is often unknown if the planulae settle and the scyphopolyps reproduce in those low-salinity waters. In the present study, scyphozoan species from the German Bight (North Sea) were tested in laboratory experiments to investigate their tolerance of low salinity. Planula larvae released from medusae in salinity 32 were still active after the salinity was reduced to 10 (Cyanea capillata, Cyanea lamarckii) and to 7 (Chrysaora hysoscella) in laboratory treatments. Planulae did not settle on the undersides of floating substrates when salinity was reduced to <20. By contrast, planulae released from C. capillata medusae in Kiel Bight (western Baltic Sea) in salinity 15 developed into polyps in laboratory cultures. Polyps reared from planulae in salinity 36 survived a reduction to 12 (C. capillata, C. lamarckii) and to 8 (Aurelia aurita). Polyps of all tested species strobilated and released young medusae (ephyrae) in salinity 12. These results show a high tolerance of planulae and polyps to low salinity, indicating their possible occurrence in estuaries and brackish waters. In addition to laboratory observations, young C. capillata ephyrae were collected in the western Baltic Sea (Kiel Bight) in salinity 15, which indicates that they were probably released by a local polyp population. We suggest that the polyps of the painfully stinging lion’s mane, C. capillata, may be more widespread in the Baltic Sea than previously assumed and that the occurrence of the medusae may not only depend on inflow of water masses from the North Sea.     

Effects of feeding regime on growth rate in the Mediterranean Sea anemone Actinia equina (Linnaeus)

Polyps of Actinia equina are the most common sea anemones in the rocky intertidal zone of the Mediterranean coast of Israel, where they occur in one of the southernmost populations of this species in the northern hemisphere. We examined effects of feeding rate on polyp growth at ambient sea temperature for this population. Under laboratory conditions, polyps were left unfed, or were fed with brine shrimp (Artemia) once every 2 weeks, once a week, or twice a week. Of the four experimental treatments, only feeding twice a week resulted in polyp growth; under all other regimes, the sea anemones lost body mass. We conclude that a high rate of feeding is required at sea temperatures in the eastern Mediterranean, where these sea anemones may have high metabolic rates relative to more northern populations.     

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.     

Bau und Lebensgeschichte des Polypen vonTripedalia cystophora (Cubozoa,class. nov., Carybdeidae) und seine Bedeutung für die Evolution der Cnidaria

FollowingHaeckel (1880), most zoologists have grouped the Cubomedusae with the class Scyphozoa. However, the actual systematic position and evolution of the Cubomedusae remained unclear because essential phenomena of the life cycle, i. e. life history and structure of the polyp generation and the process of medusa formation were unknown. Successful cultivation of the Carribean larviparousTripedalia cystophora Conant, 1898 elucidated for the first time the complete life cycle of a cubomedusa. Primary polyps could be raised from planulae which were transferred by air mail from La Parguera, Puerto Rico. The sessile polyp is solitary. Its morphology, anatomy, and behaviour are described. The body (length 0.6–1.0 mm) is radially constructed without any trace of tetramerous structures. 6 to 11 solid capitate tentacles insert in one circle, above which the body ends in a long contractile snout-like mouth cone (proboscis). The body is sac-like without gastric septa or gastric pockets; its base is enveloped by a small cup of thin, structureless periderm. Asexual reproduction by which the stock is enlarged quickly envolves lateral budding of small secondary polyps. After detachment these small polyps go through a creeping phase. The fully grown polyp shows a remarkable behavioural plasticity as it can migrate and change into an inactive encysted stage. The whole polyp metamorphoses into a single medusa. All externally visible metamorphosis phases are described. First, the polyp's body becomes tetramerous due to 4 longitudinal folds. The tentacles congregate into 4 groups, each in one quadrant. While the distal parts of the tentacles are resorbed, their bases develop into 4 perradial sensory organs (rhopalia). Interradially, 4 new tentacles are formed and become the primary tentacles of the medusa. Simultaneously, the complete body of the polyp transforms into the bell of the medusa. At the end of the metamorphosis which takes 5 to 6 days at 25 to 27° C, the young medusa begins to pulsate quickly and swims away leaving behind the empty peridermal cup. The morphology of the young medusa is described.T. cystophora has a tricnidom of basitrich haplonemes, holotrich haplonemes, and heterotrich microbasic euryteles. The ecology of both, polyp and medusa generation, is briefly outlined. A critical comparison between the polyp and medusa ofT. cystophora and the Scyphozoa and Hydrozoa reveals important differences. Consequently, a new class, Cubozoa, must be established and given the evolutionary position between Scyphozoa and Hydrozoa. Diagnoses are presented for the polyp ofT. cystophora and the class Cubozoa.