Nematocyst Types Research Articles

The marine biologist—Bob Endean

Bob Endean was a dedicated marine biologist with an extensive knowledge of coral reef communities in the Great Barrier Reef and fauna in subtropical Queensland waters. He commenced a study of venomous and poisonous marine animals dangerous to man at a time when the field was new, employing a variety of techniques to investigate the venom apparatus, mode of delivery of venom or toxin, mode of toxic action on excitable tissues, and biochemistry of venom or toxin. Determination of the pharmacological properties of crude venom from Conus marine snails advanced characterization of conotoxins by later workers. A study of four types of nematocysts from the box-jellyfish Chironex fleckeri provided information as to their structure, function, and mechanism of discharge; myotoxins T1 and T2 were isolated from microbasic mastigophores. Endean studied poisonous stonefish ( Synanceia trachynis) and, with Ann Cameron, scorpionfish ( Notesthes robusta); investigations of ciguatera and of paralytic shellfish poisoning were initiated. He organized the collection of Australian frogs which led to the isolation of caerulein by Erspamer in Italy. Endean highlighted the ecological danger of the population explosion of the crown-of-thorns starfish ( Acanthaster planci) and provided the impetus for the creation of the Great Barrier Reef Marine Park.

Nematocysts of the Cubozoa

Nematocysts (stinging organelles) are an important part of cnidarian identification, but the cnidomes of many species remain poorly known because of identification difficulties and confusing nomenclature. Currently, the cnidomes of 20 cubozoan species are documented in whole or in part (including four undescribed species and five newly described species); 18 of these are re-examined in detail, and the cnidomes of 13 species are newly presented. Type material was used for these studies where possible. A new category of nematocyst is designated, namely ‘p-rhopaloid’, characterized by having a v-shaped notch in the undischarged shaft, as in p-mastigophores, but having a lobed discharged shaft, as in rhopaloids; this type of nematocyst is found in both the Carybdeida and Chirodropida. Measurements, shape descriptions, and photographs are presented for all cnidomes studied. Also presented are a glossary to nematocyst terminology, descriptive sections on nematocyst nomenclature and preparation, and a key to the nematocysts of theCubozoa. Special remarks sections for taxonomists and forensic specialists are given, along with a summary of phylogenetic patterns. This catalogue will be useful to taxonomists, envenomation physicians, and toxinologists, as well as anyone wishing to identify cubozoan specimens or stings.

Variation in lethality and effects of two Australian chirodropid jellyfish venoms in fish

The North Queensland chirodropid box jellyfish Chironex fleckeri and Chiropsalmus sp. share similar nematocyst composition and the same prey of Acetes australis shrimps in their early medusa stages; however, as C. fleckeri individuals reach larger size, the animals add fish to their diet and their complement of nematocyst types changes, allowing larger doses of venom to be delivered to prey. This study demonstrated that the venoms of the two species differ as well: despite similar effects previously documented in crustacean prey models, the two had widely different cardiac and lethal effects in fish, with C. fleckeri being substantially more potent in its ability to cause death. Comparisons between the venom delivery abilities of the two species showed that the change in nematocysts of C. fleckeri cannot alone account for its ontogenetic shift to prey fish; instead, its prey ecology clearly necessitates it having venom capable of acting efficiently to cause death in fish. Although this venom is almost certainly produced at greater metabolic cost to the animal than the less-lethal venom of Chiropsalmus sp., owing to its greater molecular protein complexity, it confers the advantage of increased caloric intake from fish prey, facilitating larger size and potentially greater reproductive output of C. fleckeri over Chiropsalmus sp.

Nematocyst complements of nudibranchs in the genus Flabellina in the Gulf of Maine and the effect of diet manipulations on the cnidom of Flabellina verrucosa

Aeolid nudibranchs maintain functional nematocysts, which are sequestered from the nudibranchs’ cnidarian prey and provide protection against predators. Some species exhibit extensive variation in incorporated nematocysts, while others maintain a limited number of types. This study examines the apparent diversity in uptake and patterns of nematocyst incorporation among related species. Nematocyst complements were described for four Gulf of Maine nudibranch species in the genus Flabellina exhibiting a variety of feeding strategies and prey specificities. Diet manipulations were performed to examine the response to changing nematocyst availability using a generalist consumer, Flabellina verrucosa, to assess nematocyst uptake based on diet. The flabellinid species examined exhibited significant differences in nematocyst incorporation, reflecting differences in their specificity as predators and nematocyst types available in their natural prey. The nematocyst complement of F. verrucosa was the most variable and differed among collection regions. When diet was manipulated, nematocyst uptake depended on the prey the nudibranchs consumed, but when offered a variety of prey, F. verrucosa selectively preferred nematocysts from scyphistomae. The observed variation in nematocyst uptake among species and regions probably relates to environmental disparities among populations.

Morphology of the nematocysts of the medusae of two scyphozoans, Catostylus mosaicus and Phyllorhiza punctata (Rhizostomeae): implications for capture of prey

Abstract. We examined the cnidomes (total complement of nematocysts) of medusae of the zooxanthellate and azooxanthellate jellyfishes Phyllorhiza punctata and Catostylus mosaicus (Rhizostomeae, Scyphozoa), and compared the assemblage of zooplankton captured on the oral arms of each species to determine whether differences in the types or amount of zooplankton captured were consistent with possible differences in the cnidomes. Cnidomes were described using light and scanning electron microscopy. Each species had a distinct cnidome and, in general, specimens of P. punctata appeared to have far fewer nematocysts than those of C. mosaicus. Four types of nematocysts were identified in medusae of C. mosaicus; 2 types of holotrichous isorhizae, rhopaloids, and birhopaloids. In C. mosaicus, the oral arms and bell margins possessed all of these types, but the cnidomes of the 2 regions differed in relative abundances and sizes of isorhizae and rhopaloids. Five types of nematocysts were identified in medusae of P. punctata, although not all types were found in all specimens. Round holotrichous isorhizae were found only in the bell, while oval holotrichous isorhizae, rhopaloids of 2 distinct size ranges, and birhopaloids were found in the bell and oral arms. Cnidomes of the bell and oral arms in specimens of P. punctata also differed in the relative abundance and sizes of oval isorhizae and rhopaloids. Although there were clear differences in the overall cnidomes and absolute abundances of nematocysts in each species, the oral arms (feeding appendages) of specimens of both C. mosaicus and P. punctata had similar types and relative abundances of nematocysts. Zooplankton sampled from the oral arms of each species showed that both species preyed predominantly on copepod nauplii and larvae of gastropods and bivalves. Medusae of C. mosaicus captured ∼10 × more gastropod larvae and 5 × more bivalve larvae than those of P. punctata. Specimens of P. punctata captured approximately twice as many copepod nauplii as those of C. mosaicus. Differences in the relative abundance of types of zooplankton captured by each species could not be adequately explained by differences in the cnidomes of the oral arms.

A novel statistical analysis of cnidocysts in acontiarian sea anemones (Cnidaria, Actiniaria) using generalized linear models with gamma errors

Comparative studies on cnidocysts, involving adequate statistical treatment, are very scarce. Classical statistical tests are frequently used assuming normal frequency distributions of capsule lengths, but many distributions are non-normal in acontiarian sea anemones. A traditional choice in these situations are non-parametric tests, although they are not as powerful as parametric tests. An extension of classical methods was developed by some authors; these models, called Generalized Linear Models (GLM), can be used under certain conditions with non-normal data. In view of the properties of our data, that are positive, skewed and with constant coefficient of variation, a GLM with gamma distribution and inverse link function was chosen to analyse the cnidae of acontia from the species Haliplanella lineata, Tricnidactis errans and Anthothoe chilensis. Graphical analysis of residuals showed that these assumptions were reasonable. This method allowed us to avoid transformation of data set and controversial cases in the limit of significance level. For this task, appropriate subroutines in GLIM language were written. In all cases highly significant differences were found between the specimens considered for every species and nematocyst type (b-rhabdoids, p-rhabdoids B1b and p-rhabdoids B2a).

A review of zoanthid nematocyst types and their population structure

A review of zoanthid nematocyst types and their population structure

Effects of the 1997?1998 El Ni�o on the cnidarian community of a high turbidity coral reef system (northern Bahia, Brazil)

We are reporting on the results of a 4-year study that allowed for the analysis of the effects of the 1997–1998 El Nino Southern Oscillation (ENSO) event on the cnidarian community of the naturally high-turbidity reefs of northern Bahia, Brazil. Cnidarian densities were significantly different between pre- and post-ENSO years, with significant consequent changes in community composition. BIOENV analysis identified variations in turbidity, mean temperature variance, and cloud cover as the factors best explaining changes in the community. We suggest that the 1997–1998 ENSO event, the most intense on record, had a differential effect on the cnidarian community. Highest mortalities were suffered by minute hydroid colonies, partial mortality by octocorals and actiniarians, while large hydroid colonies and scleractinians were the least affected. Such an ability to survive under the stressful environmental regime imposed by this ENSO event is attributed to the presence of morphological pre-adaptations (e.g., size of colony polyps, abundance of certain nematocyst types) and the inherent phenotypic plasticity that results from long-term exposure to naturally stressful conditions.

Management of nematocysts in the alimentary tract and in cnidosacs of the aeolid nudibranch gastropod Cratena peregrina

The nudibranch gastropod Cratena peregrina (Opisthobranchia: Aeolidaceae), when feeding on polyps of the hydrozoan Eudendrium racemosum (Cnidaria: Anthoathecata), devours masses of small microbasic eurytele and holotrichous isorhiza nematocysts. Large proportions of these nematocysts were found undischarged in the alimentary tracts of the snails. Feeding experiments in this study tracked the fate of nematocysts as they passed through the alimentary canal to the digestive gland in the dorsal appendages, the cerata, to the cnidosacs, and finally in the faeces. In digestive cells, many structurally intact nematocysts were present in large phagosomes that remained unaffected even after 2 days fasting, and phagosomes containing nematocysts were found in the faeces. Thus, it is inferred that fusion of nematocyst-containing phagosomes with lysosomes and subsequent digestion of nematocysts is blocked. Masses of exposed, undigested and structurally intact nematocysts were discarded in the faeces. In the tips of the cerata, other nematocysts were phagocytosed by cnidophages and stored in the cnidosacs. After release, in contact with seawater, cnidosac nematocysts were able to discharge. When cnidophore tentacles of E. racemosum with only holotrichous isorhizas were fed to the snails, the isorhizas arrived in the cnidosacs about 2 h after feeding and mixed with existing small euryteles. Some cnidosacs also contained very large microbasic eurytele or large macrobasic eurytele nematocysts, possibly from Eudendrium ramosum and Eudendrium glomeratum, respectively. This indicates that the various types of nematocysts from food were all incorporated into the cnidosacs. Evidence for a selection process or digestion of a certain nematocyst type in the cnidophages was not obtained. It is concluded that a large proportion of the nematocysts ingested with the food are not digested, but are eliminated, structurally and functionally intact, via the alimentary canal and the tips of the cerata.

Importance of Nematocysts in Taxonomy of Acontiarian Sea Anemones (Cnidaria, Actiniaria): A Statistical Comparative Study

Many papers describe the cnidae from acontiarian sea anemone species, but comparative studies involving significant data amounts, combined with adequate statistical treatment have not been realized. The aim of the present paper is to carry out a comparative study of acontian cnidae from the species Haliplanella lineata (Verrill, 1869), Tricnidactis errans Pires, 1988 (Haliplanellidae) and Anthothoe chilensis (Lesson, 1830) (Sagartiidae). Five living specimens of each species were used; the length of 50 unfired capsules was measured and taken randomly from the following nematocyst categories: b-rhabdoids, p-rhabdoids B1b, p-rhabdoids B2a. A total of 2,000 measurements was done. The data were analyzed with descriptive statistics (mean, standard deviation, median, maximum, minimum, and semiinterquartile range) and Shapiro-Wilks test, Box-Cox transformation, Kruskal-Wallis test and single factor ANOVA. The normal distribution of the dataset must be tested for each nematocyst type in any quantitative study of the cnidae. We conclude that variation in nematocyst size should not be used as an element of conclusive value in the diagnosis of species of acontiarian sea anemones. For these purposes, other characters have to be used to define precisely each taxon, including qualitative variation of the cnidae.

Nematocyst ratio and prey in two Australian cubomedusans, Chironex fleckeri and Chiropsalmus sp.

This study examined differences in the nematocyst ratios between two species of Australian cubozoans. In Chiropsalmus sp., a species that feeds exclusively on shrimp, no changes in the ratio of the three groups of nematocyst present in the cnidome were detected with size of the individual animals. In Chironex fleckeri, the ratio of different types of nematocysts in the cnidome for small animals (less than 40 mm) was similar to that of Chiropsalmus sp. However, with an increase in body size in C. fleckeri, the nematocyst ratio changed, with mastigophores (nematocysts believed to hold the lethal venom component for prey) increasing in proportion. The change in cnidome ratio is correlated with a change in the prey of C. fleckeri with increased size. Small C. fleckeri appeared to feed exclusively on prawns, medium sized animals fed on fish and prawns and large animals fed predominantly on fish. An increase in the proportion of mastigophores (and presumably the lethal venom component) in the cnidome of C. fleckeri may also be responsible for why this species has caused numerous human fatalities, while the Australian Chiropsalmus sp. has not.

The behavioral and developmental physiology of nematocysts

Nematocysts are the nonliving secretions of specialized cells, the nematocytes, which develop from multipotent stem cells. Nematocysts are the means by which coelenterates capture prey and defend against predation. The 25 or more known types of nematocysts can be divided into to four functional categories: those that pierce, ensnare, or adhere to prey, and those that adhere to the substrate. During development a collagenous cyst, which may contain toxins, forms; a hollow thread, which becomes coiled as it invaginates, develops. Maturing nematocyte–nematocyst complexes migrate to their discharge sites and are deployed in specific patterns. The mechanisms of pattern determination are not clear. Discharge of nematocysts appears to involve increases in intracapsular osmotic pressure consequent upon release of bound calcium within the capsule; the eversion of the filament may depend upon release of structural tension consequent upon a loss of zinc from the thread. Evidence exists that discharge is initiated as a calcium-dependent exocytosis, triggered by an electrical signal resulting from the transduction of mechanical stimuli received at the nematocyte's cnidocil. Chemical signals transduced in adjacent sensory cells alter the frequency response of the nematocyte. In opposition to the nematocyte–nematocyst independent effector hypothesis, excitatory and inhibitory neuronal input appears to regulate discharge.

Morphology and distribution of a deep-water Narcomedusa (Solmarisidae) from the northeast Pacific

Specimens of Solmaris sp. (Solmarisidae, Narcomedusae) with only four tentacles were collected in the northeast Pacific. The majority were collected in Canadian Pacific waters by Tucker trawl from stations outside the 500-m contour off the west coast of Vancouver Island, British Columbia, at depths of 300-700 m. Six were collected in vertical hauls at Station P (50oN, 145oW). The oral stomach wall contains three prominent rings of tissue. There is a peripheral ring of aggregates of gonadal tissue. Nematogenic areas with three types of nematocysts form an intermediate ring closer to the mouth than the gonads, and they also overlie the gonadal position where nematogenic tissue extends out to the base of each tentacle. Immediately surrounding the mouth, the epithelium of the oral stomach wall is greatly thickened, and this central ring contains large numbers of secretory cells.

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.

Divergence of Nematocysts in Two Colour Morphs of the Intertidal Beadlet AnemoneActinia Equina

In the common intertidal sea anemoneActinia equina(Cnidaria: Actiniaria) the morphological plasticity and lack of hard parts has caused considerable debate as to what constitutes a species. Over the last several years genetic studies have indicated that this ‘species’ consists of various separate gene-pools which appear to function as cryptic biological species. Conventional taxonomy has often concentrated on the use of a cnidome, the type, structure and number of nematocysts ('stinging’ cells). However, the usefulness of nematocysts to distinguish among various morphs ofA. equinaand other anthozoan species has recently been questioned. Here we describe the first detailed study of nematocyst differences between two well characterized genetically differentiated morphs with different coloured pedal discs. Measurements were taken from each type of nematocyst in five different tissues. Contrary to expectations, clear and significant nematocyst differences were found betweenActiniawith red or pink pedal discs and others with green to grey pedal discs. These findings support previous electrophoretic studies and suggest that quantitative descriptions of the cnidome may accurately identify separate species within other genera of Anthozoa.

Cellular Origins of Kinocilia, Stereocilia, and Microvilli on Tentacles of Sea Anemones of the Genus Calliactis (Cnidaria: Anthozoa)

Sea anemones feed by orchestrated movements of tentacles covered with ciliary cones overlying both nematocytes and sensory neurons and mediating nematocyst discharge into prey. The purpose of this study was to investigate the functional morphology of tentacle sensory receptors on Calliactis parasitica and C. tricolor with a combination of scanning electron microscopy (SEM) of surface features and transmission electron microscopy (TEM) of internal cellular details. We found that the ciliary cones of two types of nematocysts differed: mastigophore-containing nematocytes had an inner ring of large-diameter stereocilia, and basitrich-containing nematocytes had small-diameter stereocilia. Two types of sensory neurons were identified: one had a ciliary cone with an inner ring of large-diameter stereocilia, and the other had a long kinocilium surrounded by a basal ring of short, stubby microvilli. Varying lengths of stereocilia on peripheral supportive cells contributed to both ciliary cones of nematocytes and sensory neurons. Both the supportive epithelial cells with stereocilia and the nonsupportive epithelial cells without stereocilia had a single long kinocilium with a basal body, an accessory centriole, and a thick striated rootlet. Gland cells had a short cilium surrounded by even shorter microvilli. Spirocysts formed apical domes on spirocytes, which had two peripheral rings of short microvilli but no cilium. We believe this combined SEM and TEM study of sensory hairs on tentacles of two species of Calliactis adds to our knowledge of ciliary structures and their cellular associations in sea anemones. Additional key words: ciliary cones, nematocytes, sensory cells, gland cells Sea anemones have feeding tentacles covered with ciliary cones which overlay nematocysts and sensory neurons (Pantin 1942). The ciliary cones have in common a kinocilium central to several rings of stereocilia of varying lengths derived from adjacent supportive cells (Mariscal 1974a,b; Peteya 1975; Mariscal & Bigger 1976). The kinocilium is characterized by a typical 9x2 + 2 pattern of microtubules, whereas the stereocilia have filamentous cores of actin similar to those of vertebrate hair cells (Watson & Roberts 1995). Ciliary cones of sea anemones have been compared to vertebrate hair bundles both morphologically and physiologically (Mariscal 1974a; Watson & Roberts 1995; Mire & Watson 1997). A directional displacement of a vertebrate hair bundle that stretches tip links between adjacent stereocilia and opens transduction channels causes depolarization of the hair cell (Osborne et al. 1984; Markin & Hudspeth 1995). Bundle deflection of sensory neuron ciliary cones having tip links between adjacent stereocilia induces ion channels a Author for correspondence. E-mail: westfall@vet.ksu.edu to open, resulting in depolarization of supportive cells on one side of the complex (Mire & Watson 1997). Ciliary cones of nematocytes and of sensory neurons in sea anemones appear similar. At first, it was believed that chemoreception of N-acetylated sugars by supportive cells caused nematocyte ciliary cones to elongate and frequency tune to movements of swimming prey, leading to discharge of nematocysts (Watson & Hessinger 1989, 1991). This view supports the independent effector hypothesis of nematocyst discharge (Pantin 1942). More recent work, using better optics, has demonstrated that the sensory neuron/supporting cell complexes respond to N-acetylated sugars and elongate their hair bundles to tune to movements of swimming prey (Mire-Thibodeaux & Watson 1994; Watson & Roberts 1995). Those studies suggested that the nervous system plays a role in nematocyst discharge. In the present study, we have used a combination of SEM and TEM to distinguish ciliary cones of sensory neurons from those of the nematocytes and to further differentiate between various kinds of nemaThis content downloaded from 157.55.39.144 on Wed, 21 Sep 2016 05:31:38 UTC All use subject to http://about.jstor.org/terms Sensory structures on tentacles of sea anemones tocytes in the genus Calliactis. We have also investigated the cellular origins of other sensory structures such as kinocilia, stereocilia, and microvilli.

Morphogenesis of the atrichous isorhiza, a type of nematocyst, in Hydra observed with a monoclonal antibody.

We produced a monoclonal antibody, AE03, which recognized mucous granules in the basal disk gland cells in Hydra and the secreted mucus with which they stick onto substrate. AE03 also recognized atrichous isorhizas, one of the four types of nematocyst present in tentacles, and their nematoblasts present in the body column. With this monoclonal antibody, we could observe the detailed morphogenesis of the atrichous isorhiza from the beginning of its formation. The elongation and invagination processes of external tubes and correspondence between the external tubes and the thread of discharged nematocysts were confirmed.

Chrysaora achlyos, a Remarkable New Species of Scyphozoan from the Eastern Pacific.

An enormous new species of scyphozoan jellyfish, Chrysaora achlyos, is described from the eastern Pacific. The description is based primarily on color photographs and video footage of living animals and the morphology of four specimens collected in 1989. The natural history, life cycle, and sporadic appearance of the species all are unknown. The species appeared most recently in large numbers in 1989 but has appeared at least twice previously in this century; published photographs (unlabeled or incorrectly identified) appeared in 1926 and 1965. The species is easily distinguished by its size and coloration from other known species in the genus, all of which are considerably smaller. Morphological characters are described, and limited data on nematocyst types are presented. Because of the size of the new species and the known potency of the sting of congeners, we mention briefly the possible consequences of human contact.

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.

Collagenaceous, thiol-containing proteins of cnidarian nematocysts: A comparison of the chemistry and protein distribution patterns in two types of cnidae

1. 1. Nematocyst structural proteins (NSP) from the sea anemones Aiptasia pallida and Metridium senile and the siphonophore Physalia physalis are primarily low molecular weight collagens linked by disulfide bonds. 2. 2. NSP patterns resolved by SDS-PAGE revealed a common, major collagen species (40 kDa) in each nematocyst type, together with other collagens and non-thiol-containing proteins. 3. 3. For each cnidarian, NSP glycosylation profiles were significantly different. 4. 4. Monoclonal antibodies against Aiptasia NSP demonstrated a differential distribution between capsule wall and thread. 5. 5. NSP differences would account for the diversity of morphologic and functional types.