Dynamic tuning of hair bundle mechanoreceptors in a sea anemone during predation

The sea anemone Haliplanella luciae (Cnidaria, Anthozoa) detects chemical and mechanical stimuli from prey. Hair bundle mechanoreceptors on the tentacles participate in regulating discharge of microbasic p-mastigophore nematocysts. Properly stimulated hair bundles sensitize the anemone to discharge nematocysts into objects that contact the tentacles. The hair bundle mechanoreceptors are composed of stereocilia derived from a multicellular complex. This complex consists of a single sensory neuron surrounded by two to four supporting cells. The mechanoreceptor is similar in many ways to vertebrate hair cells of the acousticolateralis system. However, anemone hair bundles are adjustable in structure and responsiveness according to the activity of two different chemoreceptors. One chemoreceptor binds N -acetylated sugars and the other binds amino compounds including proline. N -acetylated sugars induce lengthening of the hair bundle and a downward shift in frequencies that elicit maximal discharge of microbasic p-mastigophore nematocysts. Furthermore, N -acetylated sugars shift maximal discharge to smaller amplitude vibrations. Thus, N -acetylated sugars likely tune hair bundles so that small, swimming zooplankton stimulate maximal discharge. Proline leaks into the seawater from the hemolymph of wounded prey. Proline induces shortening of the hair bundle and shifts maximal discharge of nematocysts to higher frequencies and to larger amplitude vibrations. Thus, proline likely tunes hair bundles so that small, wounded, prey stimulate maximal discharge of nematocysts as they struggle to escape. Thus, suitably sized prey stimulate maximal discharge of microbasic p-mastigophore nematocysts upon first contacting the anemone tentacle and again upon attempting to escape.     

Effects of light and dark treatments on feeding by the reef coral Pocillopora damicornis (Linnaeus)

The feeding capability of Pocillopora damicornis (Linnaeus) was measured by exposing segments of the same colony to different densities of Artemia salina (L.) nauplii and determining the number of ingested prey. Feeding is directly related to prey density. No plateau in feeding capability was observed over the range of prey densities used.The effects of reduced photosynthesis on feeding capability and tissue dry weight were also examined in colonies maintained in unfiltered running sea water. Tissue samples from clonal segments of Pocilloporadamicornis colonies maintained in a covered (dark) sea table for 2 days or 15 to 17 days weighed significantly less than equivalent samples from segments maintained in a normal (light) sea table. Segments maintained in a darkened sea table for over 2 wk were unable to ingest as many Artemia nauplii as their light table equivalents. These data indicate that the amount of Zooplankton available to the colonies in the sea table was insufficient to meet their metabolic requirements and that feeding in Pocillopora damicornis was dependent upon energy derived from photosynthesis by the zooxanthellae.     

Prey Detection and Prey Capture in Copepod Nauplii

Copepod nauplii are either ambush feeders that feed on motile prey or they produce a feeding current that entrains prey cells. It is unclear how ambush and feeding-current feeding nauplii perceive and capture prey. Attack jumps in ambush feeding nauplii should not be feasible at low Reynolds numbers due to the thick viscous boundary layer surrounding the attacking nauplius. We use high-speed video to describe the detection and capture of phytoplankton prey by the nauplii of two ambush feeding species (Acartia tonsa and Oithona davisae) and by the nauplii of one feeding-current feeding species (Temora longicornis). We demonstrate that the ambush feeders both detect motile prey remotely. Prey detection elicits an attack jump, but the jump is not directly towards the prey, such as has been described for adult copepods. Rather, the nauplius jumps past the prey and sets up an intermittent feeding current that pulls in the prey from behind towards the mouth. The feeding-current feeding nauplius detects prey arriving in the feeding current but only when the prey is intercepted by the setae on the feeding appendages. This elicits an altered motion pattern of the feeding appendages that draws in the prey.     

Active Nematocyst Isolation Via Nudibranchs

Cnidarian venoms are potentially valuable tools for biomedical research and drug development. They are contained within nematocysts, the stinging organelles of cnidarians. Several methods exist for the isolation of nematocysts from cnidarian tissues; most are tedious and target nematocysts from specific tissues. We have discovered that the isolated active nematocyst complement (cnidome) of several sea anemone (Cnidaria: Anthozoa) species is readily accessible. These nematocysts are isolated, concentrated, and released to the aqueous environment as a by-product of aeolid nudibranch Spurilla neapolitana cultures. S. neapolitana feed on venomous sea anemones laden with stinging nematocysts. The ingested stinging organelles of several sea anemone species are effectively excreted in the nudibranch feces. We succeeded in purifying the active organelles and inducing their discharge. Thus, our current study presents the attractive possibility of using nudibranchs to produce nematocysts for the investigation of novel marine compounds.     

Organelle survival in a foreign organism: Hydra nematocysts in the flatworm Microstomum lineare

Nematocysts are characteristic organelles of the phylum cnidaria. They are designated kleptocnidae when sequestered in animals that feed on cnidaria. Kleptocnidae are known for more than a century. Nevertheless it is still enigmatic how selected nematocyst types survive in the predator and how they reach their final destination in the foreign body. In the free-living Platyhelminth Microstomum lineare the fate of nematocysts of the prey Hydra oligactis was analyzed at the ultrastructural level and by fluorescence microscopy using hydra polyps that had been stained in vivo with the fluorescent dyes TROMI and TRITC. M. lineare digested hydra tissue in its intestine within 30?min and all nematocyst types were phagocytosed without adherent cytoplasm by intestinal cnidophagocytes. Desmoneme and isorhiza nematocysts were digested whereas cnidophagocytes containing the venom-loaded stenotele nematocysts started to migrate out of the intestinal epithelia through the parenchyma to the epidermis thereby traversing the subintestinal and subepidermal muscle layer. Within one to two days, M. lineare began to form a muscle layer basolateral around epidermal cnidophagocytes. Epidermal stenoteles survived in M. lineare for at least four weeks. The ability of epidermal stenotele nematocysts to discharge suggest that this hydra organelle preserved its physiological properties in the new host.     

Bioactive Compounds of Sea Anemones: A Review

Marine organisms and their associated microorganisms contain a wide range of novel bioactive natural compounds that are widely used in the field of anti-microbial, anti-tumor, and anti-cancer drug discovery research. Hence, much focus has been given to isolate the bioactive compounds from marine sources. Sea anemone, one such marine resource, is used in recent years to extract bioactive compounds. It belongs to the phylum Cnidaria. The distinguishing feature of cnidarians is nematocysts, specialized venomous organs that the animals use mainly for capturing prey and protecting themselves from predators. There are over one thousand species of sea anemone reported worldwide and of which 40 species belonging to 17 families are found in India. Out of 40 species, 24 are marine, 13 are estuarine and 3 are common to both habitats. We present an overview of some of the potential marine bioactive compounds from a curative point of view isolated from sea anemone. Among the Order Actiniaria, Family Actiniidae exhibits by far the highest number of species yielding promising compounds, followed by Family Stichodactylidae. Haemolytic activity has been the major area of interest in the screening of actinarian compounds.

     

Discharge of nematocysts isolated from aeolid nudibranchs

Nematocysts were extracted from 3 nudibranch species and one sea anemone species, and the ability of several test fluids to promote discharge was examined. Except when isolated in sodium citrate, nudibranch nematocysts did not discharge in response to any test fluids. Nudibranch nematocysts isolated in sodium citrate discharged when tested with EGTA, distilled water, and calcium-free artificial seawater, but there were differences among the 3 nudibranch species. Nematocysts isolated from one nudibranch species and nematocysts isolated from that nudibranch's sea anemone prey differed in the percentage that discharged in response to EGTA and distilled water. These results suggest that nematocysts stored by nudibranchs are altered in some way, resulting in the different discharge responses.     

Effects of satiation and starvation on nematocyst discharge, prey killing, and ingestion in two species of sea anemone

Studies spanning 60 years with several cnidarian species show that satiation inhibits prey capture and ingestion and that starvation increases prey capture and ingestion. Most have attributed the effects of satiation to inhibition of nematocyst discharge. We hypothesized that satiation inhibits prey capture and ingestion in sea anemones (Haliplanella luciae and Aiptasia pallida) primarily by inhibiting the intrinsic adherence (i.e., holding power) of discharging nematocysts. Using a quantitative feeding assay for H. luciae, we found that satiation completely uncoupled prey killing from prey ingestion, while nematocyst-mediated prey killing was only partially inhibited. Using A. pallida to measure nematocyst discharge and nematocyst-mediated adhesive force, we showed that satiation completely inhibited the intrinsic adherence of discharging nematocysts from Type B and Type C cnidocyte/supporting cell complexes (CSCCs), while only partially inhibiting nematocyst discharge from Type Bs. These inhibitory effects of satiation were gradually restored by starvation, reaching a maximum at 72 h after feeding. Thus, the effects of satiation and starvation on prey killing and ingestion in two species of acontiate sea anemones are primarily due to changes in the intrinsic adherence of nematocysts from both Type B and Type C CSCCs.     

The nature of the adhesion to shells of the symbiotic sea anemone calliactis tricolor (Leseur)

The mechanism of tentacular adhesion to gastropod shells has been demonstrated for a symbiotic sea anemone, Calliactis tricolor (Leseur) by means of scanning electron microscopy. Both basitrichous isorhiza nematocysts and spirocysts are involved with the former being much more abundant on the shells. Contrary to its classical characterization, the thread of the basitrichous isorhiza nematocyst possesses, in addition to the large spines at its base, minute spines along its length.     

Differences in predation among morphotypes of the rotifer Asplanchna silvestrii

1. Interactions were observed between three morphotypes of the predatory rotifer Asplanchna silvestrii and six different prey (Brachionus plicatilis, B. rotundiformis, B. pterodinoides, B. satanicus, Hexarthra jenkinae and copepod nauplii) to understand the differences in feeding abilities among morphotypes that may have led to the evolution of this predator polymorphism. The outcome of predation events was affected significantly, both by predator morphotype and prey type. Predator morphotypes also interacted differently with different prey types. 2. The two smaller morphotypes, the saccate and the cruciform, responded similarly to prey overall, except that the smallest morphotype (saccate) was unable to ingest the most mobile prey (nauplii) and less able to ingest relatively large prey (B. plicatilis). The largest morphotype, the campanulate, had the highest encounter rate with prey, but the lowest probability of attack after encounter, so that it consumed far fewer prey per feeding bout than did the smaller morphotypes. This may have been because campanulates prefer larger prey than used in this study. 3. Highly mobile prey (H. jenkinae and copepod nauplii) were much less susceptible to predation than the less mobile Brachionus species. While evasiveness reduced attacks by saccates and cruciforms, campanulates did not have a significantly lower attack rate on H. jenkinae and copepod nauplii than on less evasive prey. Large body size moderately defended B. plicatilis against ingestion by saccates only. The short-spined B. satanicus was the only prey that was rejected after capture, resulting in lower ingestion probabilities for B. satanicus than other brachionid prey.     

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.     

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.     

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.     

Factors affecting zooplankton feeding by the sea anemoneAiptasia pallida

Effects of various treatments on prey capture, prey ingestion and ingestion time of individualArtemia salina nauplii by the sea anemoneAiptasia pallida Verrill were studied in the laboratory. Exposure to crudeArtemia homogenate, 5 × 10^–4 M reduced glutathione or 5 × 10^–4 M proline significantly decreased the number ofArtemia that were captured and ingested but had no significant effect on the ingestion time of individualArtemia. Multiple captures increased the total ingestion time but decreased ingestion time per prey item. Results suggest that, under these conditions, the prey capture phase of zooplankton feeding was somewhat distinct from the ingestion phase since chemical stimuli that significantly reduced prey capture had no significant effect on ingestion time.     

Neurotoxin localization to ectodermal gland cells uncovers an alternative mechanism of venom delivery in sea anemones

Jellyfish, hydras, corals and sea anemones (phylum Cnidaria) are known for their venomous stinging cells, nematocytes, used for prey and defence. Here we show, however, that the potent Type I neurotoxin of the sea anemone Nematostella vectensis, Nv1, is confined to ectodermal gland cells rather than nematocytes. We demonstrate massive Nv1 secretion upon encounter with a crustacean prey. Concomitant discharge of nematocysts probably pierces the prey, expediting toxin penetration. Toxin efficiency in sea water is further demonstrated by the rapid paralysis of fish or crustacean larvae upon application of recombinant Nv1 into their medium. Analysis of other anemone species reveals that in Anthopleura elegantissima, Type I neurotoxins also appear in gland cells, whereas in the common species Anemonia viridis, Type I toxins are localized to both nematocytes and ectodermal gland cells. The nematocyte-based and gland cell-based envenomation mechanisms may reflect substantial differences in the ecology and feeding habits of sea anemone species. Overall, the immunolocalization of neurotoxins to gland cells changes the common view in the literature that sea anemone neurotoxins are produced and delivered only by stinging nematocytes, and raises the possibility that this toxin-secretion mechanism is an ancestral evolutionary state of the venom delivery machinery in sea anemones.     

Evaluation of the grazer–prey interaction as a biotechnological strategy to increase toxin production by dinoflagellate cultures in photobioreactors

In this paper, we extend an existing approach to biotechnologically assess grazer–prey interactions between the crustacean Artemia salina (grazer) and the toxic dinoflagellate Protoceratium reticulatum (prey). The applied strategy is presented as a bioprocessing tool for enhancing the production of toxins and bioactive compounds in dinoflagellate cultures. Interactions were based on direct and indirect contact between the grazer and the prey, as well as on the use of different extracts from A. salina cysts and supernatants from cultures in which A. salina had been grown. Several treatments were found to stimulate the growth and yessotoxin production of P. reticulatum mainly due to the action of dissolved excreted substances and/or metabolites released and/or extracted from A. salina. One of the best results was obtained with a culture medium formulation containing 10 % (v/v) supernatant from a culture of A. salina nauplii. This treatment was scaled up to a 15-L photobioreactor. The average maximum specific growth rate (μ _max) of P. reticulatum in this photobioreactor, operated in batch mode, increased by 27 %, whereas the maximum cell concentration (C _max) decreased by 20 % relative to the corresponding control culture. An average increase in yessotoxin production of 50 % with respect to the control culture was observed.     

Hydroid defenses against predators: the importance of secondary metabolites versus nematocysts

Marine hydroids are commonly thought to be defended by stinging organelles called nematocysts that penetrate predator tissues and inject proteinaceous venoms, but not all hydroids possess these nematocysts. Although an increasing number of bioactive secondary metabolites have been isolated from marine hydroids, ecological roles of these compounds are poorly known. To test the hypothesis that nematocysts and noxious secondary metabolites represent alternative defenses against predation, we examined hydroids from North Carolina, United States for: (1) the palatability of whole polyps before and after nematocysts had been deactivated; (2) the palatability of their chemical extracts; and (3) their nutritional value in terms of organic content, protein content, and levels of refractory structural material (chitin). All hydroids were avoided by a generalist predator, the pinfish Lagodon rhomboides, compared with palatable control foods. Two of these (Halocordyle disticha and Tubularia crocea) became palatable after being treated with potassium chloride to discharge their nematocysts, suggesting that these species rely on nematocysts for defenses against predators. Chemical extracts from nematocyst-defended species had no effect on fish feeding. The four species that remained unpalatable after nematocysts had been discharged (Corydendrium parasiticum, Eudendrium carneum, Hydractinia symbiolongicarpus, Tridentata marginata) possessed chemical extracts that deterred feeding by pinfish. We have isolated and characterized the structures of the deterrent metabolites in two of these species. We found no differences in nutritional content or levels of chitin between nematocyst-defended and chemically defended species, and no evidence that either of these played a role in the rejection of hydroids as prey. Our results suggest that, among hydroids, chemical defenses may be at least as common as nematocyst-based defenses and that the two may represent largely alternative defensive strategies. The four hydroid species with deterrent extracts represent four families and both sub-orders of hydroids, suggesting that chemical defenses in this group may be widespread and have multiple origins. Received: 25 May 1999 / Accepted: 1 February 2000     

Prey capture capabilities by juveniles of the false percula clownfish (Amphiprion ocellaris) fed calanoid nauplii vs. adults

The reaction field of juvenile false percula clownfish (Amphiprion ocellaris) were studied when fed two different developmental stages (nauplii and adults) of the calanoid copepod Pseudodiaptomus annandalei. As the copepods undergo ontogenetic development, their morphologic and kinematic traits changes and may therefore influence the ability of the clownfish to identify and capture prey. The fish reacted to nauplii at shorter distances (15.2 ± 7.1 mm) compared to adult copepods (28.0 ± 9.8 mm). However, the fish reaction angle was significantly wider when offered nauplii (?25.3° to 64.4°) compared to adult copepods (?14.2° to 36.7°). This resulted in an equivalent attack rate on both prey items. Hence, even though nauplii are less apparent at greater distances, the fish counteract this partly by reacting to smaller prey items at a wider range. However, the carbon-specific ingestion rate was higher when offered adult copepods, which suggests adult copepods are a more rewarding prey.     

Nematocyst composition of the cubomedusan Chiropsalmus quadrigatuschanges with growth

The nematocysts of Chiropsalmus quadrigatus (Cubozoa; Cubomedusa; Chirodropidae) were examined to determine if their composition changes with an increase in body size. Fixed tentacles of specimens collected in Okinawa, Japan, were homogenized and their nematocysts were observed under a differential interference contrast microscope. Six nematocyst types were observed in medusae of all sizes microbasic mastigophores (MM), large and small trirhopaloids (lTR and sTR), holotrichous isorhizas (HI), ellipsoidal isorhizas (eI), and ovoid isorhizas (oI). Two other nematocysts, large ovoid isorhizas (loI) and microbasic euryteles (ME), were observed only in small individuals. There was also marked difference in proportion of tentacular nematocysts between small and large individuals. HI was the dominant type in small specimens, while MM and eI were predominant in large specimens. Nematocyst composition in the bell and pedalia also differed between small and large individuals. Bells of small medusae contained oI and sTR, while only oI were observed in most large individuals. The pedalia of small medusae had clusters of MM, ME, sTR, and oI. Such single clusters on pedalium bases were characteristic of small individuals. The pedalia of large individuals contained scattered oI. Tentacles of medusae are used for prey capture, so the changes in the major type of nematocysts in tentacles may reflect changes in prey type.