Length Is Associated with Pain: Jellyfish with Painful Sting Have Longer Nematocyst Tubules than Harmless Jellyfish

A large number of humans are stung by jellyfish all over the world. The stings cause acute pain followed by persistent pain and local inflammation. Harmful jellyfish species typically cause strong pain, whereas harmless jellyfish cause subtle or no pain. Jellyfish sting humans by injecting a tubule, contained in the nematocyst, the stinging organ of jellyfish. The tubule penetrates into the skin leading to venom injection. The detailed morphology of the nematocyst tubule and molecular structure of the venom in the nematocyst has been reported; however, the mechanism responsible for the difference in pain that is caused by harmful and harmless jellyfish sting has not yet been explored or explained. Therefore, we hypothesized that differences in the length of the nematocyst tubule leads to different degrees of epithelial damage. The initial acute pain might be generated by penetration of the tubule, which stimulates pain receptor neurons, whilst persistent pain might be caused by injection of venom into the epithelium. To test this hypothesis we compared the lengths of discharged nematocyst tubules from harmful and harmless jellyfish species and evaluated their ability to penetrate human skin. The results showed that the harmful jellyfish species, Chrysaora pacifica, Carybdea brevipedalia, and Chironex yamaguchii, causing moderate to severe pain, have nematocyst tubules longer than 200 μm, compared with a jellyfish species that cause little or no pain, Aurelia aurita. The majority of the tubules of harmful jellyfishes, C. yamaguchii and C. brevipedalia, were sufficiently long to penetrate the human epidermis and physically stimulate the free nerve endings of Aδ pain receptor fibers around plexuses to cause acute pain and inject the venom into the human skin epithelium to cause persistent pain and inflammation.     

Predation by the phyllosoma larva of Ibacus novemdentatus on various kinds of venomous jellyfish

The phyllosoma, a larva of spiny and slipper lobsters, has an exceptionally flat body and long appendages. It is known to associate with several species of cnidarian jellyfish, a behavior that is not rare in crustaceans. Indeed, phyllosomas clinging onto jellyfish have been observed both in the laboratory and in the natural environment. Wild phyllosomas have been found to contain jellyfish tissues in their hepatopancreas and feces, suggesting that the larvae utilize jellyfish as a food source; however, how they capture jellyfish and what species of jellyfish they prefer have rarely been investigated. The few previous studies conducted have suggested that phyllosomas have a high specificity for jellyfish (preying on only a few species); in contrast, the results of our study indicate that specificity is low. We show that phyllosomas prey on a variety of jellyfish species including deadly stinging types, on a variety of jellyfish developmental stages, and on various parts of the jellyfish body. When making contact with a jellyfish, phyllosomas first cling onto its exumbrella, feed on its tentacles or oral arms, and then consume the exumbrella. Phyllosomas may be capable of defending themselves against any types of nematocyst sting, and it is likely that they have evolved to utilize venomous jellyfish as a food in the open sea, where food may be scarce.     

Adaptable defense: a nudibranch mucus inhibits nematocyst discharge and changes with prey type

Nudibranchs that feed on cnidarians must defend themselves from the prey's nematocysts or risk their own injury or death. While a nudibranch's mucus has been thought to protect the animal from nematocyst discharge, an inhibition of discharge by nudibranch mucus has never been shown. The current study investigated whether mucus from the aeolid nudibranch Aeolidia papillosa would inhibit nematocyst discharge from four species of sea anemone prey. Sea anemone tentacles were contacted with mucus-coated gelatin probes, and nematocyst discharge was quantified and compared with control probes of gelatin only. Mucus from A. papillosa inhibited the discharge of nematocysts from sea anemone tentacles. This inhibition was specifically limited to the anemone species on which the nudibranch had been feeding. When the prey species was changed, the mucus changed within 2 weeks to inhibit the nematocyst discharge of the new prey species. The nudibranchs apparently produce the inhibitory mucus rather than simply becoming coated in anemone mucus during feeding. Because of the intimate association between most aeolid nudibranchs and their prey, an adaptable mucus protection could have a significant impact on the behavior, distribution, and life history of the nudibranchs.     

Structural and Developmental Disparity in the Tentacles of the Moon Jellyfish Aurelia sp.1

Tentacles armed with stinging cells (cnidocytes) are a defining trait of the cnidarians, a phylum that includes sea anemones, corals, jellyfish, and hydras. While cnidarian tentacles are generally characterized as structures evolved for feeding and defense, significant variation exists between the tentacles of different species, and within the same species across different life stages and/or body regions. Such diversity suggests cryptic distinctions exist in tentacle function. In this paper, we use confocal and transmission electron microscopy to contrast the structure and development of tentacles in the moon jellyfish, Aurelia species 1. We show that polyp oral tentacles and medusa marginal tentacles display markedly different cellular and muscular architecture, as well as distinct patterns of cellular proliferation during growth. Many structural differences between these tentacle types may reflect biomechanical solutions to different feeding strategies, although further work would be required for a precise mechanistic understanding. However, differences in cell proliferation dynamics suggests that the two tentacle forms lack a conserved mechanism of development, challenging the textbook-notion that cnidarian tentacles can be homologized into a conserved bauplan.     

Different nematocytes have different synapses in the sea anemone Aiptasia pallida (Cnidaria,Anthozoa)

Sea anemones feed by discharging nematocysts into their prey, but the pathway for control of nematocyst discharge is unknown. The purpose of this study was to investigate the ultrastructural evidence of neuro-nematocyte synapses and to determine the types of synaptic vesicles present at different kinds of nematocyst-containing cells. The tip and middle of tentacles from small specimens of Aiptasia pallida were prepared for electron microscopy and serial micrographs were examined. We found clear vesicles in synapses on mastigophore-containing nematocytes and dense-cored vesicles in synapses on basitrich-containing nematocytes and on one cnidoblast with a developing nematocyst. In addition, we found reciprocal neuro-neuronal and sequential neuro-neuro-nematocyte synapses in which dense-cored vesicles were present. It was concluded that : (1) neuro-nematocyte synapses are present in sea anemones, (2) different kinds of synaptic vesicles are present at cells containing different types of nematocysts, (3) synapses are present on cnidoblasts before the developing nematocyst can be identified and these synapses may have a trophic influence on nematocyst differentiation, and (4) both reciprocal and sequential synapses are present at the nematocyte, suggesting a complex pathway for neural control of nematocyst discharge. J. Morphol. 238:53–62, 1998. © 1998 Wiley-Liss, Inc.     

Prey Capture Ecology of the Cubozoan Carukia barnesi

Adult Carukia barnesi medusae feed predominantly on larval fish; however, their mode of prey capture seems more complex than previously described. Our findings revealed that during light conditions, this species extends its tentacles and ‘twitches’ them frequently. This highlights the lure-like nematocyst clusters in the water column, which actively attract larval fish that are consequently stung and consumed. This fishing behavior was not observed during dark conditions, presumably to reduce energy expenditure when they are not luring visually oriented prey. We found that larger medusae have longer tentacles; however, the spacing between the nematocyst clusters is not dependent on size, suggesting that the spacing of the nematocyst clusters is important for prey capture. Additionally, larger specimens twitch their tentacles more frequently than small specimens, which correlate with their recent ontogenetic prey shift from plankton to larval fish. These results indicate that adult medusae of C. barnesi are not opportunistically grazing in the water column, but instead utilize sophisticated prey capture techniques to specifically target larval fish.     

Ultrastructure of a novel eurytele nematocyst of Carybdea alata Reynaud (Cubozoa,Cnidaria)

The ultrastructural characteristics of nematocysts from the cubozoan Carybdea alata Reynaud, 1830 (Hawaiian box jellyfish) were examined using light, scanning and transmission electron microscopy. We reclassified the predominant nematocyst in C. alata tentacles as a heterotrichous microbasic eurytele, based on spine, tubule and capsule measurements. These nematocysts exhibited a prominent and singular stylet, herein referred to as the lancet. Discharged nematocysts from fixed tentacle preparations displayed the following structures: a smooth shaft base, lamellae, a hemicircumferential fissure demarking the proximal end of a stratified lancet, and a gradually tapering tubule densely covered with large triangularly shaped spines. The lancet remained partially adjoined to the shaft base in a hinge-like fashion in rapidly fixed, whole-tentacle preparations. In contrast, this structure was not observed in discharged nematocyst preparations which involved multiple transfer steps prior to fixation. Various approaches were designed to detect this structure in the absence of fixative. Detached lancets were located in proximity to discharged tubules in undisturbed coverslip preparations of fresh tentacles. In addition, examination of embedded nematocysts from fresh tentacles laid on polyacrylamide gels revealed still-attached lancets. To examine the function of this structure in prey capture, Artemia sp. laden tentacles were prepared for scanning electron microscopy. While carapace exteriors exhibited structures proximal to the lancet, i.e., the nematocyst capsule and shaft base, neither tubule nor lancet structures were visible. Taken together, the morphological data suggested a series of events involved in the discharge of a novel eurytele from C. alata.     

Nematocysts of Rhopilema nomadica (Scyphozoa: Rhizostomeae), an immigrant jellyfish in the eastern mediterranean

Rhopilema nomadica—a recently discovered scyphomedusa in the eastern Mediterranean—is considered a lessepsian migrant. Its nematocysts were extracted from the scapular and mouth-arm tentacles and examined using light and electron microscopy techniques. The morphometric parameters of the nematocysts were measured before and after complete discharge. Three categories of nematocysts were identified: heterotrichous isorhiza haploneme, holotrichous isorhiza haploneme, and heterotrichous microbasic eurytele. The relative abundance of the nematocysts and their occurrence in tissues of the jellyfish were noted. A brief discussion concerning the classification of certain types of nematocysts is given. A comparison with the available data on other Rhopilema species revealed that the nematocyst categories of R. nomadica are more similar to those of the Atlantic R. verrilli than to those of the Western Pacific R. esculentum. A brief comparison of the injuries caused by these species is given. © 1995 Wiley-Liss, Inc.     

Novel proteinaceous toxins from the box jellyfish (sea wasp) Carybdea rastoni

During summer and autumn, the box jellyfish (sea wasp) Carybdea rastoni is one of the most bothersome stinging pests to swimmers and bathers on the Japanese coast. Two labile but potent hemolytic toxins from the tentacles of Carybdea rastoni were isolated in their active forms using newly developed purification methods. The molecular masses of the isolated C. rastoni toxin-A and toxin-B (CrTX-A and CrTX-B) are 43 and 46 kDa, respectively, as calculated from SDS-PAGE. In the present study, we sequenced the full-length cDNA (1600 bp), which encodes both CrTX-A and CrTX-B. The deduced 450 amino acid sequence of the CrTXs, showed no significant homology with any known protein. This report presents the first complete sequence of a proteinaceous jellyfish toxin. Furthermore, it was revealed that CrTX-A was primarily localized in the nematocyst, whereas CrTX-B was detected only in the tentacle. Because the nematocyst is the organ responsible for the cnidarian sting, the remainder of the study focused on the toxicity of CrTX-A. We found that CrTX-A was fatally toxic to mice at 20 microg/kg (i.v.) and crayfish at 5 microg/kg (i.p.). Subcutaneously injected CrTX-A (0.1 microg) caused inflammation of mouse skin. These results showed that CrTX-A is responsible for the cutaneous inflammation observed in humans stung by C. rastoni.     

Isolation,characterization, and comparison of hemolytic peptides in nematocyst venoms of two species of jellyfish (Chrysaora quinquecirrha and Cyanea capillata)

• 1.1. Hemolysins of the sea nettle, Chrysaora quinquecirrha, and the lions' mane jellyfish, Cyanea capillata, collected in the Delaware Bay were partially purified by sequential gel-filtration and high performance liquid chromatography.
• 2.2. The nematocyst contents of both jellyfish had hemolytically active fractions containing large quantities of glycine and serine along with an unknown amino acid residue.
• 3.3. The Chrysaora hemolysin appeared to have a mol. wt greater than 6000 but less than 10,000 daltons.
• 4.4. Glycophorins were the most effective inhibitors to the hemolysins at the lowest concentration.

     

The cnidarian nematocyst: a miniature extracellular matrix within a secretory vesicle

Nematocysts are the taxon-defining features of all cnidarians including jellyfish, sea anemones, and corals. They are highly sophisticated organelles used for the capture of prey and defense. The nematocyst capsule is produced within a giant post-Golgi vesicle, which is continuously fed by proteins from the secretory pathway. Mature nematocysts consist of a hollow capsule body in which a long tubule is coiled up that, upon discharge, is expelled in a harpoon-like fashion. This is accompanied by the release of a toxin cocktail stored in the capsule matrix. Nematocyst discharge, which is one of the fastest processes in biology, is driven by an extreme osmotic pressure of about 150 bar. The molecular analysis of the nematocyst has from the beginning indicated a collagenous nature of the capsule structure. In particular, a large family of unusual minicollagens has been demonstrated to form the highly resistant scaffold of the capsule. Recent findings on the molecular composition of Hydra nematocysts have confirmed the notion of a specialized extracellular matrix, which is assembled during an intracellular secretion process to form the most complex predatory apparatus at the cellular level.     

Protective Effect of Tetracycline against Dermal Toxicity Induced by Jellyfish Venom

Background

Previously, we have reported that most, if not all, of the Scyphozoan jellyfish venoms contain multiple components of metalloproteinases, which apparently linked to the venom toxicity. Further, it is also well known that there is a positive correlation between the inflammatory reaction of dermal tissues and their tissue metalloproteinase activity. Based on these, the use of metalloproteinase inhibitors appears to be a promising therapeutic alternative for the treatment of jellyfish envenomation.

Methodology and Principal Findings

Tetracycline (a metalloproteinase inhibitor) has been examined for its activity to reduce or prevent the dermal toxicity induced by Nemopilema nomurai (Scyphozoa: Rhizostomeae) jellyfish venom (NnV) using in vitro and in vivo models. HaCaT (human keratinocyte) and NIH3T3 (mouse fibroblast) incubated with NnV showed decreases in cell viability, which is associated with the inductions of metalloproteinase-2 and -9. This result suggests that the use of metalloproteinase inhibitors, such as tetracycline, may prevent the jellyfish venom-mediated local tissue damage. In vivo experiments showed that comparing with NnV-alone treatment, tetracycline pre-mixed NnV demonstrated a significantly reduced progression of dermal toxicity upon the inoculation onto rabbit skin.

Conclusions/Significance

It is believed that there has been no previous report on the therapeutic agent of synthetic chemical origin for the treatment of jellyfish venom-induced dermonecrosis based on understanding its mechanism of action except the use of antivenom treatment. Furthermore, the current study, for the first time, has proposed a novel mechanism-based therapeutic intervention for skin damages caused by jellyfish stings.     

Juvenile Thalassoma amblycephalum Bleeker (Labridae, Teleostei) dwelling among the tentacles of sea anemones: A cleanerfish with an unusual client?

At least 51 species of fishes are facultative symbionts of sea anemones. Most of the behavioural, ecological and physiological aspects of these associations including their costs and benefits are unknown. We recorded the behaviour and the habitat use of eight assemblages (three or ten specimens each) of the juvenile wrasse Thalassoma amblycephalum dwelling among the tentacles of the two sea anemones Entacmaea quadricolor (clonal type), and Heteractis magnifica at a coral reef in southern Japan during 16 months in daylight hours. There are only two past records of this facultative association, one from east Africa and one from Indonesia. The wrasse remained close to and was occasionally in physical contact with the host when foraging amongst the tentacles. When frightened, they took shelter among corals, away from the host anemone. The wrasse co-existed with the anemonefishes Amphiprion frenatus in E. quadricolor and A. ocellaris in H. magnifica. By using forced host contact tests ex situ and scanning electron microscopy examination of the fish epidermis, we show that juveniles of this wrasse are protected from E. quadricolor, but possibly not from H. magnifica. We suggest that juvenile T. amblycephalum dwelling among the tentacles of sea anemones are cleanerfish with an unusual client, in that they appear to clean mucus and, or, necrotic tissue from the sea anemone host.     

The utilization of cnidarian nematocysts by aeolid nudibranchs: Nematocyst maintenance and release in spurilla

Some nudibranchs that feed on cnidarians are known to store nematocysts within cnidophage cells and use them for their own defense. Most of the nematocysts are in direct contact with the cytoplasm of the cnidophage. Nematocysts are not subjected to lysosomal enzymes because any phagocytic membrane that surrounded the nematocyst after engulfment does not persist. Cnidophage organelles are restricted to regions surrounding the nematocysts and may aid in the maintenance and development of the nematocysts. The release of cnidophages is initiated by a contraction of a dense muscle complex surrounding the cnidosac. Nematocysts do not discharge if the cnidophage membrane does not rupture upon release. A comparison of nematocyst maintenance in Spurilla neapolitana and nematocyst retention in other organisms is presented.     

The jellyfish buffet: jellyfish enhance seabird foraging opportunities by concentrating prey

High levels of jellyfish biomass have been reported in marine ecosystems around the world, but understanding of their ecological role remains in its infancy. Jellyfish are generally thought to have indirect negative impacts on higher trophic-level predators, through changes in lower trophic pathways. However, high densities of jellyfish in the water column may affect the foraging behaviour of marine predators more directly, and the effects may not always be negative. Here, we present novel observations of a diving seabird, the thick-billed murre, feeding on fish aggregating among the long tentacles of large jellyfish, by using small video loggers attached to the birds. We show that the birds encountered large jellyfish, Chrysaora melanaster, during most of their dives, commonly fed on fish associated with jellyfish, and appeared to specifically target jellyfish with a high number of fish aggregating in their tentacles, suggesting the use of jellyfish may provide significant energetic benefits to foraging murres. We conclude that jellyfish provide feeding opportunities for diving seabirds by concentrating forage fish, and that the impacts of jellyfish on marine ecosystems are more complex than previously anticipated and may be beneficial to seabirds.     

The nature of the adhesion of tentacles to shells during shell-climbing in the sea anemone Calliactis parasitica (Couch)

Phase contrast microscopy and scanning electron microscopy show that during the response of the symbiotic sea anemone Calliactis parasitica (Couch) to shells of Buccinum undatum (L.) three times as many spirocysts as nematocysts are discharged. Observations indicate that spirocysts are responsible for the adhesion of tentacles to shells.Discharge levels are not significantly influenced by the nature of the substratum to which the anemones are attached. The reported observation that fewer tentacles adhere to shells when anemones are settled on shells than when they are fixed on a different substratum is re-interpreted in terms of a new model for the control of spirocyst discharge.     

Separation and analysis of different types of nematocysts from <Emphasis Type="Italic">Cyanea capillata</Emphasis> (L.) medusae

Medusae play an important role in marine ecosystems, as competitors of many invertebrate and fish species. Additionally, jellyfish stings can cause severe pain, inflammation of the affected skin, and allergic reactions in human. Climate and environmental changes are likely to affect the medusae, but it is not yet clear whether these will affect their distribution, physiology, and their toxicity. Very little is known about the effect of biotic and abiotic factors on the proliferation and the distribution of medusan nematocysts. In this study, we compared three types of nematocysts (euryteles and A- and O-isorhizas) and venoms of Cyanea capillata medusae (Scyphozoa) obtained from the North Sea and the Baltic Sea, which have different salinity and temperature ranges. Different types of nematocysts were separated by laser microdissection and pressure catapulting (LMPC), and the proteinaceous contents of the nematocysts were analyzed by matrix-assisted laser desorption ionization time-of-flight mass spectrometry (MALDI-TOF MS). Medusae from the brackish Baltic Sea possessed more euryteles than those from the North Sea. The O-isorhizas and A-isorhizas were smaller in the Baltic Sea sample compared to the North Sea samples and the length-to-width ratios were larger in the Baltic Sea sample. Moreover, the pattern of proteins (potential toxins) obtained from the separated nematocysts showed differences among samples and nematocyst types, but no clear pattern was observable. This study displays the novel LMPC/MALDI-TOF MS approach as a useful tool to investigate the function and venom of cnidarian nematocysts types.     

Behavioural response of the scyphozoan jellyfish Aurelia aurita (L.) upon contact with the predatory jellyfish Cyanea capillata (L.)

Underwater manipulative experiments were carried out in situ to investigate the sensibility of the jellyfish Amelia aurita (L.) to contact with the tentacles of Cyanea capillata (L), commonly known as a predator on A. aurita. Movements of individual medusae touched by tentacles of C. capillata and other objects were video‐recorded during SCUBA dives. The behavioural variable studied was change in swim pulse frequency. The results showed that A. aurita was highly susceptible to the tentacles of C. capillata and responded with an increased swim pulse frequency when touched at the umbrellar margin but not at the central exumbrella. Contact with other objects also induced a behavioural response in A. aurita.