Subumbrellar Cavity Research Articles

Jet-paddling jellies: swimming performance in the Rhizostomeae jellyfish Catostylus mosaicus.

Jellyfish are a successful and diverse class of animals that swim via jet propulsion, with swimming performance and propulsive efficiency being related to the animal's feeding ecology and body morphology. The Rhizostomeae jellyfish lack tentacles but possess four oral lobes and eight trailing arms at the centre of their bell, giving them a body morphology quite unlike that of other free-swimming medusae. The implications of this body morphology on the mechanisms by which thrust is produced are unknown. Here, we determined the wake structure and propulsive efficiency in the blue-blubber jellyfish Catostylus mosaicus (order: Rhizostomeae). The animal is propelled during both bell contraction and bell relaxation by different thrust-generating mechanisms. During bell contraction, a jet of fluid is expelled from the subumbrellar cavity, which results from the interaction between the counter-rotating stopping (from the preceding contraction cycle) and starting vortices, creating a vortex superstructure and propulsion. This species is also able to utilise passive energy recapture, which increases the animal's swimming velocity towards the end of the bell expansion phase when the bell diameter is constant. The thrust produced during this phase is the result of the flexible bell margin manoeuvring the stopping vortex into the subumbrellar cavity during bell relaxation, enhancing its circulation, and creating a region of high pressure on the inner surface of the bell and, consequently, thrust. These mechanisms of thrust generation result in C. mosaicus having a relatively high propulsive efficiency compared with other swimmers, indicating that economical locomotion could be a contributing factor in the ecological success of these medusan swimmers.

First Record of Box Jellyfish, Carybdea brevipedalia (Cnidaria: Cubozoa: Carybdeidae) from Korean Coastal Waters: Morphology and Molecular Descriptions

We firstly described a box jellyfish, Carybdea brevipedalia collected from the southern coasts of Korea. It is morphologically characterized by gastric phacellae, a special digestive system of cubozoan jellyfish, and velarium, the thin muscle flap forming the opening of the subumbrellar cavity. The phacellae are linear-shaped, comprising numerous cirri branched from multiple roots. Each root also has multiple numbers of cirrus bundles. Basis of velarial cannels parts into two branches in each octant of velarium. Its geographic distributions were limited to Jejudo and the middle-southern coasts where the organisms are seriously hazardous to bathers in summer. Numerous individuals and/or large-sized populations were observed specifically from beaches at Jeju-do, Namhae-do and a small fishing port of Namildae, while only a small amount of the individuals was observed in Gamak Bay, Jaran- Goseung Bay, and Geoje-do. We confirmed molecular identity of the Korean C. brevipedalia with comparison of nuclear ribosomal DNA sequences. Until now, Carybdea brevipedalia is the only cubozoan species reported to be distributed in Korean waters.

Divergent evolution of medusozoan symmetric patterns: Evidence from the microanatomy of Cambrian tetramerous cubozoans from South China

Living medusozoans and their Middle Cambrian ancestors are characterized fundamentally by four-fold symmetry. The symmetric pattern of their earlier antecedents during the Ediacaran–Cambrian transition, traditionally expected to be tetramerous, needs to be reconsidered in the light of Cambrian pentamerous fossil medusozoans. Here we present a microanatomic analysis of three tiny tetramerous specimens from the Lower Cambrian Kuanchuanpu Formation in southern China; they display diagnostic characteristics of Cubomedusae, including paired but well-separated interradial tentacles deep in the subumbrellar cavity, interradial septa connected by claustra, coronal muscles at the subumbrella, and an annular velarium suspended by twelve frenula. These fossils likely represent three new taxa of a monophyletic stem group of cubomedusans, which is further confirmed by our phylogenetic analysis based on the data matrix with 25 taxa and 107 characteristics. Among these fossil cubozoans and co-occurring pentamerous forms, the specimen ELISN31-31 is mostly close to the crown-group Cubomedusae with regard to its narrow vascular cavity and the endodermic perradial fusion. Diverse symmetrical patterns among different lineages of early Cambrian medusozoan candidates might have been independently evolved in different classes of medusozoans.

Lagrangian coherent structures in low Reynolds number swimming

This work explores the utility of the finite-time Lyapunov exponent (FTLE) field forrevealing flow structures in low Reynolds number biological locomotion. Previous studies ofhigh Reynolds number unsteady flows have demonstrated that ridges of the FTLEfield coincide with transport barriers within the flow, which are not shown by amore classical quantity such as vorticity. In low Reynolds number locomotion (O(1)–O(100)), in which viscous diffusion rapidly smears the vorticity in the wake, the FTLEfield has the potential to add new insight to locomotion mechanics. The targetof study is an articulated two-dimensional model for jellyfish-like locomotion,with swimming Reynolds number of order 1. The self-propulsion of the model isnumerically simulated with a viscous vortex particle method, using kinematicsadapted from previous experimental measurements on a live medusan swimmer. Theroles of the ridges of the computed forward- and backward-time FTLE fields areclarified by tracking clusters of particles both backward and forward in time. It isshown that a series of ridges in front of the jellyfish in the forward-time FTLEfield transport slender fingers of fluid toward the lip of the bell orifice, which arepulled once per contraction cycle into the wake of the jellyfish, where the fluidremains partitioned. A strong ridge in the backward-time FTLE field reveals apersistent barrier between fluid inside and outside the subumbrellar cavity. Thesystem is also analyzed in a body-fixed frame subject to a steady free stream,and the FTLE field is used to highlight differences in these frames of reference.

Kinematic properties of the jellyfish Aurelia sp.

A new, relatively simple method for determining the kinematic properties of jellyfish is presented. The bell movement of the scyphomedusa (Aurelia sp.) during its pulsation cycle was analysed using computer-aided visualization. Sequences of video images of individual Aurelia in a large aquarium were taken using a standard video camera. The images were then processed to obtain time series of the relative positions of selected points on the surface of the medusa’s bell. The duration of the bell relaxation was longer than that of the bell contraction, thereby confirming published results. In addition, the area of the exumbrellar surface of Aurelia increased during bell relaxation by more than 1.3-times that of the exumbrellar surface area during the maximum contraction of the bell. The volume change during the bell pulsation cycle was also measured using the same visualization method. Significant changes, of up to 50%, in the subumbrellar cavity volume were revealed while, in contrast, the volume between the exumbrellar and subumbrellar surfaces generally remained unchanged during the entire pulsation cycle of the bell. Comparison of the time series of the exumbrellar surface area and of the subumbrellar cavity volume indicated that the change of volume takes place before the change of the surface area of the bell.

Obelia (Cnidaria, Hydrozoa, Campanulariidae): a microphagous, filter-feeding medusa

Obelia is used in many zoology textbooks to exemplify the Hydrozoa life cycle. The body plan of Obelia medusae, however, is unique among the Hydrozoa. Contrary to all other hydromedusae, Obelia medusae do not derive from a medusary nodule, have neither a velum nor a subumbrellar cavity, the umbrella is flat, and swimming is achieved by umbrellar flapping and does not involve jet propulsion. The medusae of most Obelia species do not grow well on a diet of Artemia salina nauplii, the usual food for laboratory-reared hydrozoans, and their rearing is often difficult. Previous observations reported that Obelia medusae might eat phytoplankton, driven to the mouth by movements of both the bell and the tentacles. To evaluate the efficiency of this feeding mechanism, we gave a suspension of genetically modified Escherichia coli expressing GFP to starved, newly released medusae of both O. dichotoma and Clytia hemisphaerica (the other campanulariid genus with medusae). Obelia medusae are able to concentrate bacteria in their gastric cavity, whereas Clytia medusae are not. Contrary to other Hydromedusae that are macrophagous, Obelia is a microphagous and filter-feeding medusa, at least at the onset of its medusan life. As Cnidaria evolved before their current metazoan prey, their ancestral diet was probably microphagous. Obelia’s microphagous feeding habits could thus represent an example of the ancestral feeding condition in Cnidaria, but the apomorphic characters of its medusa suggest that its body architecture is not ancestral, and that its microphagy evolved relatively recently.

Symbiotic associations between crustaceans and gelatinous zooplankton in deep and surface waters off California

Using a remotely operated submersible (ROV) in the sea off Monterey, California, we collected deep-living zooplankton and observed their associations with crustacean symbionts. Little is known about the nature of these symbioses. Among the most interesting findings was the description of a previously unknown modality of symbiosis of the deep-living copepod Pseudolubbockia dilatata Sars. It was recorded within the subumbrellar cavity of three specimens of the bathypelagic hydromedusa Aegina citrea Eschscholtz at depths of 606–1,098 m. One of these medusae hosted a mating pair of adult copepods along with the remains of their molts corresponding to copepodid stages CV of the female and CII, CIII, CIV, and CV of the male; another medusa had an adult female, and molts of a female CV and of male CIII, CIV and CV copepodids. Our data indicate that the medusae were occupied first by an early male copepodid, and then the female joined as a CV. The presence of an adult female alone with its CV molt in a third medusa suggests that females invade the host regardless of the presence of the male in it. The medusa represents a protected environment for these copepods during vulnerable stages or processes (molting and mating). We also observed 13 new associations between hyperiid amphipods and gelatinous zooplankton at different depths. These involve four new records among members of the Infraorder Physosomata, for which only six other associations were known, and five species of amphipods and six hosts among the gelatinous zooplankton not previously recorded as symbionts. Data are provided on three families of Hyperiidea for which symbiotic associations were hitherto unknown. The ROV represents a valuable tool for the observation and sampling of these associations, whose existence has been known for a long time, but which are still poorly understood.

Kinematic analysis of swimming in Australian box jellyfish, Chiropsalmus sp. and Chironex fleckeri (Cubozoa, Cnidaria: Chirodropidae)

AbstractLocomotion of the box jellyfish Chiropsalmus sp. (cf quadrigatus)1 (Haeckel) and Chironex fleckeri (Southcott) was analysed using digital video. Specimens of Chiropsalmus sp. and C. fleckeri were collected in 2001 and 2002, respectively, from coastal waters of Northern Queensland, Australia. Chiropsalmus sp. animals were videoed swimming in an aquarium, and C. fleckeri in a large outdoor tank. Locomotor sequences of nine Chiropsalmus sp. and seven C. fleckeri individuals were analysed using video techniques. A subset of animals had fluorescent dye injected into the sub‐umbrellar cavity, to allow observation of water movements during ejection from the bell. Both species used an intermittent style of jet propulsion similar to that documented for some other species of cubozoan medusae. Computer analysis allowed examination of positions of bell parts over time intervals (0.04 s) by comparing coordinates of nodes marked on various bell parts using imaging software. Examination of node coordinates allowed a detailed qualitative description of gait, in addition to quantitative statistical analyses. General linear modelling showed that interspecific differences in locomotion were explicable in terms of body size. Larger animals of both species tended to swim faster, and with a lower pulse frequency, than smaller individuals. Smaller animals also tended to swim faster relative to their bell diameter.

The modulus of elasticity of fibrillin-containing elastic fibres in the mesoglea of the hydromedusaPolyorchis penicillatus

Hydromedusan jellyfish swim by rhythmic pulsation of their mesogleal bells. A single swimming muscle contracts to create thrust by ejecting water from the subumbrellar cavity. At the end of the contraction, energy stored in the deformation of the mesogleal bell powers the refilling stage, during which water is sucked back into the subumbrellar cavity. The mesoglea is a mucopolysaccharide gel reinforced with radially oriented fibres made primarily of a protein homologous to mammalian fibrillin. Most of the energy required to power the refill stroke is thought to be stored by stretching these fibres. The elastic modulus of similar fibrillin-rich fibres has been measured in other systems and found to be in the range of 0.2 to 1.1 MPa. In this paper, we measured the diameters of the fibres, their density throughout the bell, and the mechanical behaviour of the mesoglea, both in isolated samples and in an intact bell preparation. Using this information, we calculated the stiffness of the fibres of the hydromedusa Polyorchis penicillatus, which we found to be approximately 0.9 MPa, similar in magnitude to other species. This value is two orders of magnitude more compliant than the stiffness of the component fibrillin microfibrils previously reported. We show that the structure of the radial fibres can be modelled as a parallel fibre-reinforced composite and reconcile the stiffness difference by reinterpreting the previously reported data. We separate the contributions to the bell elasticity of the fibres and mesogleal matrix and calculate the energy storage capacity of the fibres using the calculated value of their stiffness and measured densities and diameters. We conclude that there is enough energy potential in the fibres alone to account for the energy required to refill the subumbrellar cavity.

Hyperoche shihi sp. nov. (Crustacea : Peracarida : Amphipoda): a symbiont of a deep-living medusa in the Gulf of California

From samples of deep-water zooplankton obtained in the Gulf of California, an undescribed species of the genus Hyperoche Bovallius was collected. The new species is similar to Hyperoche medusarum Kroyer and Hyperoche luetkenides Walker. It differs from its congeners mainly by the strong, large chela of pereopod 2 and the absence of processes or denticles along the posterior distal margin of same structure. It was collected at a depth of 1136 m as a symbiont of the bathypelagic hydromedusa Chromatonema erythrogonon (Bigelow). The amphipod remained grasped to the medusa subumbrellar cavity. Seven other associations are known between hyperiids and jellies in the Gulf of California, most from the epipelagic layer. This is the only deep-living species of Hyperoche known.

Non-released cryptomedusoid in the life cycle of Antennella sp. (Cnidaria, Hydrozoa, Halopterididae) from La Réunion, Indian Ocean

Summary Specimens of Antennella sp. were collected by scuba diving during the austral summer on the outer slope of the fringing reefs located on the western coast of La Réunion (55°30′E, 21°50′S) where the species forms microscopic colonies on red algae. A fertile colony was kept alive in a closed system in the laboratory. Like other Antennella species, it exhibits hermaproditism and sexual dimorphism: gonangia of both sexes are on the same stem, with female gonothecae being clearly bigger than male. In both sexes we observed cryptomedusoids with a subumbrellar cavity, an eccentric spadix surrounded by the gametes and a ring of refringent corpuscles on top. Male gonothecae have a compact blue-grey homogeneous mass of spermatozoa while females contain circa five white-opaque oocytes with a clearly visible darker nucleus. When the gametes were mature, one day after collection, medusoid tissues slid towards the base of the gonotheca in both sexes. Female gametes remained free inside the gonotheca while spermatozoa were liberated in the aquarium and fertilized oocytes. Several embryos at different stages of embryonic development (from morula to blastula) were incubated in a single gonotheca. The planula was not observed. This study revealed a previously undescribed pattern of sexual reproduction in the family Halopterididae involving unreleased cryptomedusoids instead of fixed sporosacs. This may be a more advanced regression stage of the medusa than free cryptomedusoids encountered in related families.

The role of Cnidaria in evolution and ecology

The recent setting of specific features of the Cnidaria into evolutionary and ecological frameworks suggests the centrality of this phylum in many fields of the life sciences. From an evolutionary point of view, the Cnidaria, with their diploblastic planulae, might represent the ancestral state of higher Metazoa in the light of a peramorphic origin of animal complexity from a simple, individual organism. Medusan development in the Hydroidomedusae via a medusary nodule, furthermore, implies the formation of a third tissue layer (the muscle layer lining the subumbrellar cavity). Cnidarian polyps are diploblastic, whereas at least some of their medusae are triploblastic: the evolutionary enigma of the passage from a diplo‐ to a triploblastic organisation takes place every time hydrozoan polyps bud medusae! Cnidarian polyps have also the premises of the skeletal architecture of higher animals: their chiti‐nous or carbonatic skeletons are similar to those of arthropods and vertebrates respectively. From an ecological point of view, the coelenterates probably play roles that are much more important than usually perceived. Both Cnidaria and Ctenophora feed on the eggs and larvae of most benthic, planktonic and nektonic organisms and might be crucial (with a keystone role?) in maintaining biodiversity high, by feeding on potentially monopolising species. The efficiency of gelatinous predators becomes evident during periodic outbreaks of their populations, with serious implications even on fisheries yields, demonstrating that their impact can be higher than ours!

Swimming medusoid gonophores in two species of Sertularella (Cnidaria, Hydrozoa, Sertulariidae) from Réunion Island, Indian Ocean

Summary Two life cycle patterns predominate in thecate hydroids, those with alternating polyp and medusa stages, and those with fixed gonophores. Relatively few species release short-lived medusoids, also called swimming gonophores, that carry the gametes. In the family Sertulariidae, with its large number of taxa, this mode of metagenesis has been documented previously for only two species. It is described here for two others, Sertularella diaphana (Allman, 1885) and Sertularella n. sp., from the coastal waters of Reunion Island. Freshly collected fertile male and female colonies released medusoids near dawn, one per gonotheca. Strong contractions of the bell in the swimming movements induced the shedding of gametes. Once gametes were shed, medusoids quickly degenerated and died. The medusoids were similar morphologically in these two related species, and no obvious sexual dimorphism was noted. They were ovoid in shape, the spadix was eccentric, and a velum was present; but they lacked a mouth, tentacles, sense organs, and radial and circular canals as described earlier in Amphisbetia operculata (Linneus, 1758) and Sertularia marginata Kirchenpauer, 1864. However, the medusoids described here lacked exumbrellar nematocysts. Moreover, the spadix with its dense mass of gametes was different from all other described in being stuck from base to top on one side of the subumbrella in spite of hanging freely in the subumbrellar cavity. The hypothesis that this unusual reproductive mode in sertulariids has been underestimated is confirmed by these findings.

The cnidarian premises of metazoan evolution: From triploblasty, to coelom formation, to metamery

The hydromedusan subumbrellar muscle tissues originate from a mass of endo‐ and ectoderm derived cells proliferating inwardly. This mass of cells, called entocodon, is separated by the ecto‐and endoderm through a layer of extracellular matrix, thus forming a locally triploblastic arrangement of tissues. By cavitation and differentiation, the entocodon gives rise to the striated and smooth muscle layers of the subumbrella. The structure of the striated muscle is histologically identical to that described for triploblasts, where striated muscle is mainly mesodermic. Together with the mode of development, this suggests that not all Cnidaria are diploblastic and that the subumbrellar cavity is a coelom‐like structure. The subumbreHar cavity is formed late in ontogeny, whereas the coelom in higher animals is normally formed during embryonic development. Instead of remaining closed, the subumbrella becomes open, with the muscular mesothelium in contact with the environment. This view of cnidarian structures can be pushed further while considering the regulation of modularity and metamery. The occurrence of homeotic genes in cnidarians and other ‘lower’ animals shows that the specification of body architecture has a common molecular ground throughout the animal kingdom. It is suggested that the expression of homeotic genes while specifying a given architecture might be regulated by iteration of their activity, leading to ‘low’ modular organisms and to ‘higher’ metameric ones. Replicated parts as modules and metameres might be analogous, but the affinity in their molecular specification (and possibly regulation) might indicate homology. The number of resemblances between cnidarians and ‘higher’ metazoa suggests that this phylum might be a centre of metazoan radiation, having structures which represent the living premises of the main steps of animal evolution.

The life cycle of Sertularia marginata Kirchenpauer, 1864 (Cnidaria: Hydrozoa): a medusoid-producing sertulariid

Laboratory observations showed that Sertularia marginata, a nearly cosmopolitan coastal water hydroid, produces medusoids with gametes around the manubrium. The dioecious, short-lived and rudimentary medusoid has a velum with a circular aperture, but lacks radial and circular canals, mouth, tentacles, statocysts and ocelli. Many small microbasic mastigophore nematocysts are evenly distributed on the exumbrella, except in a band near the umbrella margin. The gametes do not fill completely the sub-umbrellar cavity and are liberated with vigorous contraction of the bell, usually soon after the release of the medusoid. Spent medusoids can live for more than two hours. Fertilization occurs after release. Amphisbetia operculata is the only other known sertulariid which releases medusoids. The occurrence of medusoids in the family Sertulariidae could prove to be more common than hitherto suspected, as the life cycles of other species are closely investigated.

The Ultrastructure of the Radial Neuromuscular System of the Jellyfish Liriope tetraphylla (Hydrozoa, Trachymedusae): Implications in Crumpling Behavior.

The ultrastructure of the radial neuromuscular system of the trachymedusa Liriope tetraphylla was examined to determine the morphological substrate underlying crumpling behavior--the folding of the margin into the subumbrellar cavity by radial muscle contraction. These contractions are produced by the four smooth muscle bands that run the length of the peduncle and extend over the subumbrellar surface to the margin, along the radii. Axons are present in the radial system and attain appreciable density at the base of insertion of the peduncle; contact between this radial nerve net and the inner nerve ring may occur at the margin. Gap junctions were not encountered within the ectodermal radial system. These various observations are discussed with respect to the control of crumpling in this and other species of hydromedusae.

Cytological changes during the metamorphosis from the cubopolypTripedalia cystophora (Cubozoa, Carybdeidae) to a medusa

The life cycle ofTripedalia cystophora includes a sessile saclike polyp — the asexual reproducing form — and a pelagic tetraradial medusa — the sexually reproducing generation. Medusan development can be induced by temperature increase. It reveals neither budding nor strobilation, but a real metamorphosis of a polyp to only one medusa. According to morphological and anatomical criteria the metamorphosis can be subdivided into four different stages: (1) four longitudinal furrows segment the polyp, the tentacles of which are apportionated on the four quadrants of the body. (2) The subumbrellar cavity develops by invagination of the peristom; the relicts of the fused tentacles change to four rhopalia buds. (3) Medusan architecture including four new interradial tentacles, four rhopalia and the subumbrellar swimming musculature is completed. (4) A young tetraradial medusa starts swimming. Ultrastructural analysis of those metamorphic stages show the different processes of morphogenesis: (a) Gastrodermal cells — absorptive and spumous cells — undergo transdifferentiation and proliferation to medusan cells of the same structure and function. (b) Epidermal cells, excluding the epithel muscle cells, dissociate and are autolytically withdrawn. Dedifferentiated epithel muscle cells — interstitial cells — regain the ability to develop a complete new set of somatic cells, not originally present in the polyp. They include amongst others cross-striated muscle cells, medusan typic nematocyts and particularly sensory and nervous cells. Those cells establish a nervous system with lens-eyes, simple ocelli, statocysts, diffuse nerve net and an additional nerve ring.

On Young Stages of Limnocodium and Geryonia

ABSTRACT Metschnikoff, in a paper in the ‘Zeitsch. wiss. Zoologie,’ 1874, p. 17, describes and figures the development of Geryonia from the egg up to the formation of tentacles and an umbrella cavity. It is, however, obvious from his figures and description that certain steps in the development were not followed by him with precision—and some of his observations are supplemented, whilst others are contradicted, by those of Fol (‘Jen. Zeitsch.,’ vol. vii). It appears to be certain, from the observations of both Metschnikoff and Fol, that in Geryonia the endoderm forms by delamination1—the embryo being, when it has so formed, a nearly spherical “diblastula” without orifice of any description (Metschnikoff’s plate ii, fig. 7). The outer layer now grows away from the inner, which remains in the form of a lenticular sac, closely applied to one pole of the ectodermal sphere. From this point forwards the accounts of Haecke] Jenaische Zeitschrift,’ vol. ii), of Metschnikoff, and of Fol, are diverse. A mouth is formed by a breaking through into the endodermal sac, and a sub-umbrellar cavity is formed, and also a velum and tentacles; but the accounts given of the mode of origin of these parts is not conclusive in any one of the authors’ memoirs above cited. Haeckel observed Geryonia embryos, in which he definitely states that the sub-umbrellar cavity existed in the form of a closed sac. Metschnikoff thinks this an erroneous observation, and due to a mistaking of the endoderm sac for the sub-umbrellar cavity. According to Metschnikoff, the ectoderm and endoderm are ruptured at the central point where the enclosed endoderm sac is resting on the inner wall of the larger ectodermal sac, and the ectoderm is invaginated to form the sub-umbrellar cavity. At the same time a ring grows up at some distance from the mouth thus formed, which becomes the margin of the umbrella, and gives off, on its adoral side, the velum; on its aboral side, the first tentacles.